Individuality across environmental context in Drosophila melanogaster

Abstract Over the past decade, several studies have demonstrated that idiosyncratic animal behaviors remain consistent over long time periods. The consistency of individually variable behaviors over time is often referred to as an animal’s individuality, or if consisting of multiple traits personality. However, most experimental studies have focused on individuality in a single, well-defined environmental context, whereas it is well-established from population studies that animal behavior is highly context-dependent. The ‘person-situation debate’ in humans and decades of observations of animal individuality under intrinsically variable natural conditions raise the question of whether and to what extent animal behavior remains stable across different situations, such as changing environmental contexts. For instance, one individual might be generally more visually guided than another, or rely only on one particular visual cue, or even on this very cue only in a specific environmental context. Here, we use a combination of both well-established and novel behavioral assays to demonstrate the relationship between individual behavior and variable environmental context under tightly controlled laboratory conditions in the model system Drosophila melanogaster. The consistency of three individual traits (termed exploration, attention, and anxiety) was investigated under changing environmental contexts (temperature, visual cues, arena shape), in both walking and flying flies. We find that individuality is highly context-dependent, but even under the most extreme environmental alterations tested, consistency of behavioral individuality always persisted in at least one of the traits. Furthermore, our quantification reveals a hierarchical order of environmental features influencing individuality. We confirmed this hierarchy using a generalized linear model and a hierarchical linear mixed model. In summary, our work demonstrates that, similar to humans, fly individuality persists across different contexts, and individual differences shape behavior across variable environments, thereby making the underlying developmental and functional mechanisms amenable to genetic dissection.