Animals navigate their surroundings in a large variety of environments, ranging from dim forests at night to bright open fields during the day. How have their brains evolved to achieve precise visually guided behaviors in such different environments? Despite their small eyes and tiny brains, insects perform sophisticated orientation behaviors in almost all ecological niches on Earth. This, and their experimental accessibility, make them ideal models to pursue the aim of the proposed experiments: to reveal the neural principles that allow animal brains to produce precise navigational commands within specific environments, despite limited and often noisy sensory information. We will study the central complex (CX), a highly conserved brain region involved in sensory integration and motor planning across insects. In locusts and monarch butterflies the CX likely serves as an internal compass during migration, and CX-neurons are highly conserved between these two species, despite 360 million years of evolutionary distance. We now hypothesize that the CX underlies general orientation behavior in all insects. We will test this using electrophysiology and comparative neuroanatomy, first verifying the functional ground plan of the CX suggested by its conserved morphology. We will study two species of bees, which are non-migratory, share similar behavioral strategies, but inhabit vastly different environments (nocturnal vs diurnal). We will develop a novel virtual reality arena to present natural skylight cues combined with classic visual stimuli, all mimicking the natural habitats of both species. We will then characterize how each species’ lifestyle has shaped the neural circuitry of the CX for optimal performance in its particular ecological niche. By linking the ecology of a species to specific neural circuits, we hope to gain pioneering insights into higher visual processing in nocturnal animals and elucidate fundamental neural principles of sensory-motor transformation.