Adaptions of the peripheral visual system to dim light in hawkmoths (Sphingidae)

Dim light bears challenges for insect color vision. Both in level and spectrum, the light available drastically changes, for example at sunset and in starlight conditions, and tends to be shifted towards longer wavelengths (LW). Hawkmoths (Sphingidae) have evolved several neural adaptations enabling them to use vision for foraging and color processing at extremely low light levels. Here, we investigate if and how the peripheral visual system, notably via opsin sensitivity tuning, may act as a potential adaptation to use LW-shifted dim light. With visual modeling, we first predict achromatic and chromatic detection of a variety of flower colors when viewed under daytime, sunset, and starlight conditions by diurnal and nocturnal species. We show that while floral chromatic detection is significantly better for a green receptor (530 nm) when including all color categories, a long wavelength shift (>xxx nm) significantly improves achromatic stimuli discrimination. For colors innately attractive to hawkmoths, our modelling results further indicate that a shifted LW-sensitive receptor can increase achromatic detection of flowers in dim-light without decreasing chromatic detection of important color cues. We then characterize the spectral sensitivity of LW sensitive opsins for representative diurnal and nocturnal species across the family via eye RNA-seq analyses and in vitro heterologous expression. We show that diurnal species have retained a green-sensitive LW opsin, whereas preliminary data suggest a LW shift at least in some nocturnal species. Combined, this indicates that while chromatic cues are better processed by the green receptor typical of many diurnal insects, LW-shifted sensitivity in nocturnal species can improve flower detection in dim-light, thereby suggesting that opsin tuning may contribute a peripheral adaption mechanism to dim light vision in some nocturnal hawkmoths.