Genetic heterogeneity alleviates behavioral trade-off between exploration and vigilance in Drosophila

Abstract

Trade-offs between conflicting behaviors fundamentally constrain animal performance, yet group living can alter how such trade-offs are expressed and alleviated. Here, we disentangled the effects of aggregation and heterogeneity, both arising from group living, on the exploration-vigilance trade-off in Drosophila. Using 78 genetically distinct strains from the Drosophila Genetic Reference Panel, we compared behavioral responses of single individuals, homogeneous groups (six individuals from the same strain), and heterogeneous groups (three individuals from each of two distinct strains) under predator-like looming stimuli. Pareto optimization analysis revealed that aggregation increased both exploratory and vigilance behavior, thereby exposing the underlying exploration-vigilance trade-off. In contrast, heterogeneity enhanced group performance beyond expected levels, alleviating the cost of balancing exploration and vigilance. To identify the phenotypic basis of this alleviation, we developed a phenome-wide higher-level association study (PheHAS) that screened 190 phenotypes across strain pairs. We found that heterogeneity in activity patterns and morphological traits promoted trade-off alleviation, whereas similarity in infection responses also contributed, suggesting that social facilitation may contribute. Our study provides the first explicit demonstration that aggregation and heterogeneity exert distinct effects on a group-level behavioral trade-off and introduces PheHAS as a generalizable framework for identifying the phenotypic bases underlying diversity effects in animal groups.