The neuroethology of collective decision-making in the desert locust

Abstract

Swarms of the migratory desert locust Schistocerca gregaria can extend over several hundred square kilometers, and starvation compels this ancient pest to devour everything on its path. However, despite the plague's enormous socio-economic impact, estimated to affect ten percent of humanity, little is known about its collective decision-making processes. In this thesis, I investigate how locusts integrate different sources of information – personal experience and social cues – to make context-dependent decisions during foraging, collective motion, and escape. The resulting coupling across scales, from the neural basis of sensing to individual and collective decision-making, can be understood best through an integrative approach. For this reason, I combine behavioral assays, immersive virtual reality experiments, functional imaging, and computational modeling of decision-making processes to investigate how individual decisions in changing social contexts can scale into coordinated group behavior. In CHAPTER I, we explore the extent to which inherently selfish and cannibalistic locusts utilize social information during foraging and how they benefit from integrating this information with their personal experiences. Our results suggest that the social context strongly influences individual decisions. At the same time, their personal experience dynamically updates their behavior, resulting in split groups under symmetric and consensus under asymmetric patch conditions. Further, we modeled locust decision-making using a Bayesian framework and revealed that congruent cues reinforce decisions while incongruent ones are balanced, resulting in more optimal choices. This chapter shows that locusts readily use social information during foraging and highlights how social interactions can enhance their foraging efficiency. In CHAPTERS II and III, we pioneered techniques for targeted in vivo functional calcium imaging and introduced CalciSeg as a corresponding analysis tool to build on the findings from CHAPTER I. Specifically, we took a comparative approach between the two social phenotypes of locusts to explore how neuronal processes adapt to changing social environments during foraging. Our results from behavioral experiments suggest that olfactory social cues are critical for locust foraging decisions. Thus, we introduced targeted in vivo functional calcium imaging at the antennal lobe ensemble level to investigate how neuronal processes adapt to changing social environments during foraging. We discovered that the synergistic interactions between distinct neuronal motifs in response to food and social odors form the basis of a crowding-induced modulation of activity across the locust’s antennal lobe. In CHAPTER IV, we transition from studying foraging behavior to examining marching behavior to understand locust collective motion better. This study disentangles the positive correlation of animal density with inter-animal alignment by placing real locusts in an immersive virtual environment. We complement this approach with field and large-scale laboratory experiments to revise prevailing models for explaining collective motion. We discovered that vision is both necessary and sufficient for maintaining collective motion, while optical flow cues alone do not drive social interactions. Instead, locust marching behavior is explained by a density‑independent cognitive “ring‑attractor” framework that encodes bearings to neighbors and integrates sensory information to guide directional decisions. In CHAPTER V, I present unpublished yet highly promising data on how locusts use different information classes for escape decisions and whether the response propagates within the swarm as a behavioral contagion. To this end, we placed locusts in a virtual environment and tested how the animals respond to nearing danger, the escape response of others, or a combination of both. Our preliminary data indicate that locust escape decisions are context-dependent and based on a density-dependent modulation of sensory processing. Complementing this with large-scale behavioral experiments and extracellular nerve recordings in tethered "escaping" animals will provide valuable insight into their collective decision-making. With my thesis, I unite a diverse set of approaches within a framework that focuses on the integration of personal and social information. Overall, my work improves our understanding of desert locusts as a socio-economically relevant collective phenomenon. I demonstrate how linking sensory adaptations to behaviorally relevant tasks can improve our understanding of social modulation in non-model organisms. Thus, my findings and tools have broader implications beyond locusts, especially for elucidating olfactory-guided social behaviors in other species.