Adaptations for gas exchange enabled the elongation of lepidopteran proboscises

The extensive biodiversification of butterflies and moths (Lepidoptera) is partly attributed to their unique mouthparts (proboscis [Pr]) that can span in length from less than 1 mm to over 280 mm in Darwin’s sphinx moths. Lepidoptera, similar to other insects, are believed to inhale and exhale respiratory gases only through valve-like spiracles on their thorax and abdomen, making gas exchange through the narrow tracheae (Tr) challenging for the elongated Pr. How Lepidoptera overcome distance effects for gas transport to the Pr is an open question that is important to understanding how the Pr elongated over evolutionary time. Here, we show with scanning electron microscopy and X-ray imaging that distance effects on gas exchange are overcome by previously unreported micropores on the Pr surface and by superhydrophobic Tr that prevent water loss and entry. We find that the density of micropores decreases monotonically along the Pr length with the maxima proportional to the Pr length and that micropore diameters produce a Knudsen number at the boundary between the slip and transition flow regimes. By numerical estimation, we further show that the respiratory gas exchange for the Pr predominantly occurs via diffusion through the micropores. These adaptations are key innovations vital to Pr elongation, which likely facilitated lepidopteran biodiversification and the radiation of angiosperms by coevolutionary processes. •Butterflies and moths have micropores on the proboscis that facilitate gas exchange•Micropore density relates to proboscis length and is highest in long proboscises•Gas exchange through the micropores occurs primarily by diffusion•The tracheae of the insect body and proboscis is superhydrophobic Jiang et al. show that the proboscises of butterflies and moths have micropores that connect to the superhydrophobic proboscis tracheae and provide gas exchange via diffusion. They demonstrate the respiration abilities of the proboscis and suggest the micropores as a key innovation that facilitated proboscis elongation over evolutionary time.