Integration of parallel pathways for flight control in a hawkmoth reflects prevalence and relevance of natural visual cues

Abstract

An animal’s behaviour is the result of multiple neural pathways acting in parallel, receiving information across and within sensory modalities at the same time. How these pathways are integrated, particularly when their individual outputs are in conflict, is key to understanding complex natural behaviours. We investigated this question in the visually guided flight of the hummingbird hawkmoth Macroglossum stellatarum . These insects were recently shown to partition their visual field, using ventrolateral optic-flow cues to guide their flight like most insects, while the same stimuli in the dorsal visual field evoke a novel directional response. Using behavioural experiments which set the two pathways into conflict, we tested whether and how the ventrolateral and dorsal pathway integrate to guide hawkmoth flight. Combined with environmental imaging we demonstrate that the partitioning of the visual field followed the prevalence of visual cues in the hawkmoths’ natural habitats, while the integration hierarchy of the two pathways matched the relevance of these cues for the animals’ flight safety, rather than their magnitude in the experimental setup or in natural habitats. These results provide new mechanistic insights into the vision-based flight control of insects, and link these to their natural context. We anticipate our findings to be the starting point for comparative investigations into parallel pathways for flight guidance in insects from differently structured natural habitats.