Insect olfaction and the evolution of receptor tuning

Insects detect odorants primarily using odorant receptors (OR) housed in the dendritic membrane of olfactory sensory neurons (OSN). Pioneering studies indicated that insects, like mammals, detect odorants in a combinatorial fashion with a specific odor ligand activating several broadly tuned ORs, and each OR being activated by several ligands. Several recent studies, however, challenge this view by providing examples where ecologically relevant odorants are detected by high-specificity ORs activating dedicated neuronal circuits. Here we review these contrasting findings on the ligand selectivity of insect ORs and their neuronal wiring, and outline scenarios describing how adaptive and neutral evolution might shape both narrow and broad receptor tuning. The fact that not all ORs display narrow tuning might partly be due to key ligands having been missed from screens or too high stimuli concentrations being used. However, the birth-and-death model of OR evolution, involving both adaptive and neutral events, could also explain the evolution of broad tuning in certain receptors due to positive selection or relaxed constraint. If the insect olfactory system indeed contains both narrowly and broadly tuned ORs, this suggests that it is a hybrid between dedicated channels and combinatorial coding. The relative extent of the two coding modes is then likely to differ between species, depending on requirements of perceived chemical space and the size of the OR repertoire. We address this by outlining scenarios where certain insect groups may be more likely to have evolved combinatorial coding as their dominant coding strategy. Combinatorial coding may have evolved predominantly in insects that benefit from the ability to discriminate between a larger number of odorants and odor objects, such as polyphagous or social species. Alternatively, combinatorial coding may have evolved simply as a mechanism to increase perceived odor space in species with small OR repertoires.