To jump or not to jump: Comparing effects of phenotypic plasticity on the visual responses and escape behavior of locusts and grasshoppers

Abstract Locusts exhibit remarkable phenotypic plasticity changing their appearance and behavior from solitary grasshoppers to gregarious locusts when population density increases. These changes include morphological differences in the size and shape of brain regions, but little is known about plasticity within individual neurons and alterations in behavior not directly related to aggregation or swarming. We examined looming escape behavior and the properties of a well-studied collision-detection neuron in gregarious and solitarious animals of three closely related species, the desert locust (Schistocerca gregaria), the Central American locust (S. piceifrons) and the American bird grasshopper (S. americana). For this neuron, the lobula giant movement detector (LGMD), we examined dendritic morphology, membrane properties, gene expression, and looming responses. Gregarious animals reliably jumped in response to looming stimuli, but surprisingly solitarious desert locusts did not produce escape jumps. These solitarious animals also had smaller LGMD dendrites. This is the first study done on three different species of grasshoppers to observe the effects of phenotypic plasticity on the jump escape behavior, physiology and transcriptomics of these animals. Surprisingly, there were little differences in these properties between the two phases except for behavior. For all the three species, gregarious animals jumped more than solitarious animals, but no significant differences were found between the two phases of animals in the electrophysiological and transcriptomics studies. Our results suggest that phase change impacts mainly the motor system and that the physiological properties of motor neurons need to be characterized to understand fully the variation in jump escape behavior across phases. New & Noteworthy (74 words): Swarming is observed in some grasshopper species, called locusts. We compared jump escape behavior between gregarious and solitarious grasshoppers and locusts, as well as LGMD responses to looming stimuli, and analyzed the morphological differences in this neuron. This study provides insights into the effects of phase change on the visual system of locusts and grasshoppers as it relates to looming-evoked jump escape behavior. In this context, our results suggest that phenotypic plasticity mainly impacts the motor system. Competing Interest Statement The authors have declared no competing interest. Footnotes ↵* co-senior authors