Behavioral individuality is a consequence of experience, genetics and learning

Abstract

ABSTRACTGenetic determinism of behavior supposes that behaviors are fundamentally defined by genetics1–3. However, behaviors are also modified by development4, environment5, 6, and learning7–9. It is assumed that if we could control all of these factors, behavior would be genetically predictable. These factors, however, cannot be controlled in humans, and have been impervious to dissection and joint control even in animal models10–17. How genotype13and life experience16interact to shape individual behavior through learning17has been lacking experimental evidence, and thus remains only hypothesized8. Here, we design an experimental platform which allowed for multi-generational control over genetics, development, environment and experience. We measure learning-dependent individuality and its sources across thousands of genetically diverseDrosophila. We show that genetics plays an essential role in shaping the distributions of individual behaviors. Further, we find that genotype-specific bias shapes individual experience, which in concert with learning, causes dynamic evolution and diversification of individual behavior, even in a uniform environment. We experimentally derive that individual past life experience, genetics, and learning, in this order, shape the momentary individual expression of behavior. Finally, while association studies frequently report the opposite, we show experimentally that life experience severely diminishes the predictive power of genetics for individual learning-dependent behavior.