Behavioral individuality is a consequence of experience, genetics and learning

Abstract

Genetic determinism of behavior supposes that behaviors are fundamentally defined by genetics. However, behaviors are also modified by development, environment, and learning. 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 models. How genotype and life experience16 interact to shape individual behavior through learning has been lacking experimental evidence, and thus remains only hypothesized. 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 diverse Drosophila. 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.