The Neurobiology of a Transformation from Asocial to Social Life During Swarm Formation in Desert Locusts

Abstract

Many species display complex social interactions and for such animals other members of their species can form a major or even dominant part of their environment. Social interactions between these animals can induce long-lasting changes in brain function and behaviour that in turn alter the ways in which they respond to each other. Locusts are insects that can change reversibly between an asocial solitarious phase and a social gregarious phase that is driven by changes in population density. Phase change encompasses both a socially driven mechanism and multifaceted changes in behaviour, physiology, neurochemistry, brain morphology and even appearance. At low densities, locusts occur in the solitarious phase. Their biology is governed by the need to be inconspicuous and they actively avoid other locusts, thus maintaining their low population density. When sheer population size and scarce resources force solitarious locusts together despite their aversion to each other, a transformation is triggered that results in the gregarious phase. The stimuli responsible for starting this transformation are provided by other locusts, notably mechanosensory stimulation resulting from inadvertent jostling of each other. After just a few hours these stimuli induce changes in behaviour, including, critically, a change toward a propensity to be attracted towards other locusts. This attraction initiates a positive feedback loop whereby the continual presence of other locusts provides the necessary stimuli to drive the process towards the extreme gregarious phenotype and eventually to swarming. The biology of gregarious locusts is then dominated by the demands of group living. There is intense competition for resources and considerably greater sensory complexity in the environment brought about by living in a constantly moving throng of other animals. These behavioural demands are reflected in the substantially larger brains of gregarious locusts compared with solitarious locusts. Phase differences can also be detected at the level of identified neurons and circuits and in dramatic changes in neurochemistry, but only serotonin shows a substantial increase during the critical 1–4 h window during which gregarious behaviour is established. Blocking the action of serotonin or preventing its synthesis prevents behavioural gregarization. Applying serotonin or its agonists induces gregarious behaviour even in locusts that have never encountered other locusts. The analysis of phase change in locusts provides insights into a feedback circuit between the environment and the neurobiology of social interaction. Remarkably, there is emerging evidence that the neuronal mechanisms underlying this transformation in locusts show similarities with those underlying social behaviours in other animals.