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We used a population biological approach to assist our understanding of the evolution of behaviour, with island bumblebees as our model system. The widespread European species Bombus terrestris occurs on all major Mediterranean, and some Atlantic islands. Bees from different populations differ in a variety of behavioural traits, including floral colour preferences, flower detection, and learning behaviour. We attempted to correlate these behavioural differences with each population’s environment, but could not find straightforward adaptive explanations. We also performed reciprocal transplant studies to compare nectar foraging performance of bees from three different populations, but found that non-native bees consistently outcompeted native bees. Thus, we consider genetic drift, exaptation, and pleiotropy as possible alternative explanations to a strictly adaptive explanation for between population …