Dual olfactory pathway in Hymenoptera: Evolutionary insights from comparative studies

In the honeybee (Apis mellifera) and carpenter ant (Camponotus floridanus) the antennal lobe output is connected to higher brain centers by a dual olfactory pathway. Two major sets of uniglomerular projection neurons innervate glomeruli from two antennal-lobe hemispheres and project via a medial and a lateral antennal-lobe protocerebral tract in opposite sequence to the mushroom bodies and lateral horn. Comparison across insects suggests that the lateral projection neuron tract represents a special feature of Hymenoptera. We hypothesize that this promotes advanced olfactory processing associated with chemical communication, orientation and social interactions. To test whether a dual olfactory pathway is restricted to social Hymenoptera, we labeled the antennal lobe output tracts in selected species using fluorescent tracing and confocal imaging. Our results show that a dual pathway from the antennal lobe to the mushroom bodies is present in social bees, basal and advanced ants, solitary wasps, and in one of two investigated species of sawflies. This indicates that a dual olfactory pathway is not restricted to social species and may have evolved in basal Hymenoptera. We suggest that associated advances in olfactory processing represent a preadaptation for life styles with high demands on olfactory discrimination like parasitoism, central place foraging, and sociality.

► In the honeybee antennal lobe glomeruli connect to the mushroom bodies via two tracts.
► A similar dual olfactory pathway is present in ants and solitary advanced Hymenoptera.
► One of two investigated sawflies (Symphyta) was found with a dual olfactory pathway.
► The lateral pathway may represent a preadaptation that evolved in basal Hymenoptera.
► A dual pathway may enhance olfactory processing, discrimination and learning.