Constraints on oviposition learning: innate preference, cue integration and experience in a generalist fruit fly

Learning enables animals to adjust behavior in changing environments, yet it may be constrained by innate preferences and prior experience. We examined how these factors interact in oviposition site selection-a key fitness-related trait-in the highly polyphagous Mediterranean fruit fly, Ceratitis capitata. We addressed three questions: (i) whether learning depends on the strength of innate preferences; (ii) how visual and olfactory modalities contribute to learning; and (iii) whether egg laying is required to induce persistent preference changes. Using 3D-printed artificial fruits differing in color and olfactory cues, we showed that oviposition behavior was highly plastic but strongly constrained. Learning depended on innate preference strength: it was limited when innate preferences were strong, yet facilitated when they were weak. Both visual and olfactory cues supported learning, but only when the identity of both stimuli was consistent between conditioning and test phases. Importantly, the absence of egg-laying opportunity induced avoidance of associated sensory stimuli rather than attraction to them when oviposition opportunity is present, indicating that the outcome of an oviposition attempt strongly influences subsequent oviposition preferences. Our findings show that oviposition learning results from interactions among innate preferences, sensory integration, and associative reinforcement. These constraints have implications for understanding how generalist insects can use various host species throughout their life and how environments shape those decisions. In particular, it underlines that integrating experience-dependent changes in behavior is needed to improve behavioral pest management strategies.