Fitness landscapes reveal context-dependent benefits of oviposition behaviour

Resource choice behaviour has enormous fitness consequences and can drive niche expansion. However, individual behavioural choices are often mediated by context, determined by past experience. Do such context-dependent behaviours reflect maladaptive variation, or are they locally adaptive? Using Tribolium castaneum (the red flour beetle), we demonstrate that context-dependent oviposition behaviour reflects distinct, context-specific local fitness peaks. We measured offspring fitness to generate fitness landscapes as a function of all possible oviposition behaviours (i.e., combinations of fecundity and resource preference) in a habitat containing optimal and suboptimal resource patches. We did this by experimentally manipulating female egg allocation across patches, which allowed us to assess behaviours not typically observed in the laboratory. We found that females from different age and competition contexts exhibit distinct behaviours which optimize different fitness components, linked in a tradeoff. With prior exposure to strong competition and increasing age, females produce few but fast-developing offspring that are advantageous under high resource competition. In contrast, young naïve females produce significantly more (but slower-developing) offspring, which is beneficial under weak competition. Systematically mapping complete context-dependent fitness landscapes is thus critical to infer behavioural optimality and offers predictive power in novel contexts.