Neuromechanics of insect pollination: tactile sensing and learning in nocturnal insects

Abstract

How insects find and feed on flowers is crucial for plant pollination. Plants provide several chemical and visual cues to attract insects. However, even as insects find their host flowers, they have the additional challenge of targeting a tiny nectary opening on floral surfaces to reach the sugary reward. This becomes especially challenging for moths and butterflies because they use a long and flexible mouthpart called proboscis to draw the nectary. Additionally, nocturnal hawkmoths feed while hovering in front of flowers, often at very low lights levels during nighttime. How do moths target the tiny nectary hole in flowers, despite the low visual resolution of the nectary opening? We tracked the motion of hawkmoth proboscis as they fed from artificial, 3D-printed flowers and show that hawkmoths systematically explore floral surfaces to detect tactile features such as curvatures to target the nectary. We found that over repeated visits, they preferentially explore in ways that increases the efficiency of finding the nectary. Systematic exploration and targeting objects in the environment require expert control over appendage movements. How do hawkmoths sense and control the proboscis motion to achieve such precise movements? Pilifers are paired bristled organs at the proboscis base and are well placed to provide proprioceptive feedback about relative movements of the proboscis. To study the role of pilifers as proprioceptive organs, we drove lateral motions of the proboscis in anaesthetized head-fixed moths while simultaneously recording neural responses from the pilifer nerve. Our recordings reveal that pilifer mechanosensory neurons are sensitive to lateral motions, either to the left or to the right. Like other mechanosensory organs, they respond extremely rapidly, often within a few milliseconds. We build neural models which reveal that the neural filtering properties such as the stimulus feature and selectivity function of the pilifer mechosensors are strikingly like other insect mechanosensors, including the strain sensors on wings and halteres, abdominal mechanosensors etc. suggesting an important role for sensor mechanics and motion in encoding relevant information.