The lepidopteran analyst: how caterpillars, moths and butterflies encode taste identity and valence

The sense of taste is crucial for butterflies and moths to accomplish important life tasks such as feeding or selecting suitable oviposition sites. In Lepidoptera taste is of special importance since they are constantly confronted with a vast amount of plant secondary metabolites combined with sugars, amino acids and other primary metabolites that they need to fuel their metabolism. The high importance of many tastants for feeding and oviposition gives these compounds a strong innate meaning for the animal. During associative learning this positive or negative valence often functions as reward or punishment, giving the sense of taste an important role during memory formation. In this review we first address some general mechanisms of gustatory detection before focusing on the taste system of caterpillars and adult Lepidoptera specifically. We list recent examples of receptor genes for which the main ligands have been identified, but place special emphasis on the neuronal and behavioral responses to different tastants. Thereafter the detection of primary and secondary metabolites is reviewed, with a focus on the role of secondary plant metabolites during host-plant choice. Finally, we compiled different results on the taste processing in the lepidopteran brain and highlight the role of taste during associative learning. In this review we combined information on the role of taste for both innate and learned responses of Lepidoptera to their environment, aiming to provide a starting point for further explorations into this essential sensory modality.