Many animals form groups or societies that exhibit characteristic group behavior, called collective behavior. Collective behavior is typically seen in the coordinated shoaling behavior of fish or social division of labor of eusocial insects and differs from simple sums or averages of individuals. The principles and parameters of individual behavior that enable collective behavior have been elucidated through mathematical modeling and observational empirical studies. However, genetic substrates underlying collective behavior remain largely unknown. Here, by extending the genome-wide association analysis that has been limited to the individual to the population level, we aimed to reveal the molecular mechanism of collective behavior and gain a detailed understanding of its evolutionary processes. In this study, we focused on the collective freezing behavior of the model organism Drosophila melanogaster when exposed to visual stimuli. With a panel of 104 inbred strains with known genomic backgrounds, we tracked flies’ behavior and quantified fear response and social behavior in group experiments. In our experimental setup, flies were subject to looming stimuli for 5 min (20 trials of a black circle expanding within 500 ms on a white background every 15 sec) after a non-stimulating term for 5 min. We confirmed the fear response toward threatening stimuli, as observed in the significant reduction in locomotor activity. We also observed “group effects”, which mitigate the fear response of flies when surrounded by conspecifics, and this effect was likely achieved by the visual response to motion cues of others. The threshold of the visual response varied among strains, and we conducted genome-wide association analysis to detect genetic variants likely associated with the trait. Those hit above the genome-wide significance level included genes involved in the development of eyes and visual neurons. We are now working on the functional studies of the candidate genes, which can further deepen our understanding of the molecular mechanism of flies’ social interaction that improves group performance.
Genes underlying social collectives of flies under visual threat