Neurogenomic and behavioral principles shape freezing dynamics and synergistic performance in Drosophila melanogaster

Collective behavior plays a vital role in detecting and evading predators, yet its neural and genetic underpinnings remain poorly understood. In Drosophila melanogaster, visual cues from conspecifics can alleviate freezing responses to threatening stimuli. Using a large-scale behavioral experiment combined with GWAS, we identify key loci, including Ptp99A and kirre, which are involved in visual neuron development and may influence visual responsiveness to conspecifics. Single-cell transcriptomics and functional assays confirm the modulatory roles of Ptp99A in gene expression in visual neurons and behavior. Furthermore, mixed-strain groups show enhanced freezing behavior compared to homogeneous groups, demonstrating a "diversity effect" where genetic diversity within groups induces flexible behavioral changes. Animal-computer interaction experiments using predatory spiders validate that variation in freezing durations among interactive individuals improves antipredator behavioral performance in fly groups. Agent-based simulations further support the hypothesis that behavioral synchronization among genetically diverse individuals improves group-level performance. We introduce genome-wide higher-level association study to find loci whose genetic diversity correlates with diversity effect, highlighting the potential roles of neuronal diversity. These findings demonstrate how genetic diversity fosters synergistic responses to threats, offering insights into the neural and genomic mechanisms underlying collective behavior in non-eusocial insects.