To safely navigate their environment, flying insects rely on visual cues, such as optic flow. Which cues insects can extract from their environment depends closely on the spatial and temporal response properties of their visual system. These in turn can vary between individuals that differ in body size. How optic flow-based flight control depends on the spatial structure of visual cues, and how this relationship scales with body size, has previously been investigated in insects with apposition compound eyes. Here, we characterised the visual flight control response limits and their relationship to body size in an insect with superposition compound eyes: the hummingbird hawkmoth Macroglossum stellatarum. We used the hawkmoths’ centring response in a flight tunnel as a readout for their reception of translational optic flow stimuli of different spatial frequencies. We show that their responses cut off at different spatial frequencies when translational optic flow was presented on either one, or both tunnel walls. Combined with differences in flight speed, this suggests that their flight control was primarily limited by their temporal rather than spatial resolution. We also observed strong individual differences in flight performance, but no correlation between the spatial response cutoffs and body or eye size.

Flying animals require sensory feedback on changes of their body position, as well as on their distance from nearby objects. The apparent image motion, or optic flow, which is generated as animals move through the air, can provide this information. Flight tunnel experiments have been crucial for our understanding of how insects use optic flow for flight control in confined spaces. However, previous work mainly focused on species from two insect orders: Hymenoptera and Diptera. We therefore set out to investigate whether the previously described control strategies to navigate enclosed environments are also used by insects with a different optical system, flight kinematics and phylogenetic background. We tested the role of lateral visual cues for forward flight control in the hummingbird hawkmoth Macroglossum stellatarum (Sphingidae, Lepidoptera), which possesses superposition compound eyes, and has the ability to hover in addition to its capacity for fast forward flight. Our results show that hawkmoths use a similar strategy for lateral position control to bees and flies in balancing the magnitude of translational optic flow perceived in both eyes. However, the influence of lateral optic flow on flight speed in hawkmoths differed from that in bees and flies. Moreover, hawkmoths showed individually attributable differences in position and speed control when the presented optic flow was unbalanced.

Animals vary widely in body size within and across species. This has consequences for the function of organs and body parts in both large and small individuals. How these scale, in relation to body size, reveals evolutionary investment strategies, often resulting in trade-offs between functions. Eyes exemplify these trade-offs, as they are limited by their absolute size in two key performance features: sensitivity and spatial acuity. Due to their size polymorphism, insect compound eyes are ideal models for studying the allometric scaling of eye performance. Previous work on apposition compound eyes revealed that allometric scaling led to poorer spatial resolution and visual sensitivity in small individuals, across a range of insect species. Here, we used X-ray microtomography to investigate allometric scaling in superposition compound eyes—the second most common eye type in insects—for the first time. Our results reveal a novel strategy to cope with the trade-off between sensitivity and spatial acuity, as we show that the eyes of the hummingbird hawkmoth retain an optimal balance between these performance measures across all body sizes.

Animals vary widely in body size across and within species. This has consequences in large and small individuals for the function of organs and body parts. How these scale in relation to body size reveals evolutionary investment strategies, often resulting in trade-offs between functions. Eyes exemplify these trade-offs, as they are limited by their absolute size in two key performance features: sensitivity and spatial acuity. Previous studies of the 3D structure of apposition compound eyes, which are ideal models for allometric studies due to their size polymorphism, revealed that allometric scaling improves both local resolution and visual sensitivity in larger bumblebees (Taylor et al., 2019). Here, we build on the established methods and results to investigate allometric scaling in superposition compound eyes – the second prominent eye type in insects – for the first time. Our research highlights a surprising strategy to cope with the challenge to sensitivity and spatial resolution in small eyes, as we show that the eyes of the hummingbird hawkmoth retain an optimal balance of these performance measures across all body sizes.