Neurogenomic diversity enhances collective antipredator performance in Drosophila

Collective behavior is a unique social behavior that plays crucial roles in detecting and avoiding predators. Despite a long history of research on the ecological significance, its neural and genetic underpinnings remain elusive. Here we focus on the mesmerizing nature that visual cues from surrounding conspecifics alleviate the fear response to threatening stimuli in Drosophila melanogaster . A large-scale behavioral experiment and genome-wide association analysis utilizing 104 strains with known genomes uncovered the genetic foundation of the emergent behavioral properties of flies. We found genes involved in visual neuron development associated with visual response to conspecifics, and the functional assay confirmed the regulatory significance of lamina neurons. Furthermore, behavioral synchronization combined with interindividual heterogeneity in freezing drove nonadditive, synergistic changes in group performance for predatory avoidance. Our novel approach termed genome-wide higher-level association study (GHAS) identified loci whose within-group genetic diversity potentially contributes to such an emergent effect. Population genetic analysis revealed that selective pressure may favor increased responsiveness to conspecifics, indicating that by-productive genomic diversity within the group leads to a collective phenomenon. This work opens up a new avenue to understand the genomics underpinning the group-level phenotypes and offers an evolutionary perspective on the mechanism of collective behavior.