Stay clear and dry! How microstructure diversity can offset the hydrophobicity costs of transparency in clearwing Lepidoptera

ABSTRACT Living organisms are submitted to multiple developmental and selective constraints resulting in evolutionary compromises, one of the best examples being the integument (the outer protective layer of living organisms) which is fundamentally multifunctional. Integument anti-wetting or hydrophobicity – evolved in relation to complex and various structures - is a crucial property as it serves multiple functions like self-cleaning, locomotion, or defence against pathogens and may interfere with other functions like thermoregulation or communication. Elucidating the structure-property relationships and unravelling potential trade-offs is crucial to understand the evolution of the integument. In opaque Lepidoptera, wing scales actively contribute to anti-wetting. In clearwing Lepidoptera, wing scales are often reduced, raising the question of whether they can maintain similar hydrophobicity levels to those of opaque species and if not, whether wing microstructure (scale density, shape, insertion, and coloration) may mitigate the costs of a lower hydrophobicity. To answer these questions, we measure static contact angle (CA) of water droplets at different stages of evaporation in opaque and transparent patches of 23 Lepidoptera species that show a high diversity in wing microstructure. More specifically, we find that transparency is costly for hydrophobicity, and that such cost depends on wing microstructure. In general, transparent patches lose more hydrophobicity with water evaporation than opaque patches. Yet, this loss of hydrophobicity is attenuated for higher scale densities, erect scales compared to flat scales, coloured scales (for erect scales), multiple scale layers (for flat scales), or when combining two types of scales (piliform and lamellar) than having only one type of scale (piliform or lamellar). Nude membranes show the lowest hydrophobicity values. We find that wing hydrophobicity negatively relates to optical transparency, showing a trade-off between optics and hydrophobicity. Moreover, we find that tropical species have higher hydrophobicity in their transparent patches than temperate ones, suggesting transparent patches are under stronger selection for hydrophobicity in tropical than in temperate species. These novel findings, which are consistent with the physics of hydrophobicity, suggest that insect wings are evolutionary multifunctional compromises.