Wing transparency in butterflies and moths: structural diversity, optical properties, and ecological relevance

Abstract

In water, transparency seems an ideal concealment strategy, as testified by the variety of transparent aquatic organisms. By contrast, transparency is nearly absent on land, with the exception of insect wings, and knowledge is scarce about its functions and evolution, with fragmentary studies and no comparative perspective. Lepidoptera (butterflies and moths) represent an outstanding group to investigate transparency on land, as species typically harbor opaque wings covered with colored scales, a key multifunctional innovation. Yet, many Lepidoptera species have evolved partially or fully transparent wings. At the interface between physics and biology, the present study investigates wing transparency in 123 Lepidoptera species (from 31 families) for its structural basis, optical properties, and biological relevance in relation to visual detection (concealment), thermoregulation, and protection against UV. Our results suggest that transparency has likely evolved multiple times independently. Efficiency at transmitting light is largely determined by clearwing microstructure (scale shape, insertion, coloration, dimensions, and density) and macrostructure (clearwing area, species size, or wing area). Microstructural traits, scale density and dimensions, are tightly linked in their evolution, with different constraints according to scale shape, insertion, and coloration. Transparency appears highly relevant for concealment, with size-dependent variations. Links between transparency and latitude are consistent with an ecological relevance of transparency in thermoregulation, and not so for protection against UV radiation. Altogether, our results shed new light on the physical and ecological processes driving the evolution of transparency on land and underline that transparency is a more complex coloration strategy than previously thought.

Mimicry can drive convergence in structural and light transmission features of transparent wings in Lepidoptera

“…Here, we describe some species with coloured erected scales that are completely perpendicular to the wing membrane, such as in the ithomiine Methona curvifascia , and some species with transparent scales. Both these features were reported in transparent Lepidoptera only recently ( Gomez et al, 2021 ). Other means of achieving transparency reported in the literature are not observed among our species (e.g.…”

“…Other means of achieving transparency reported in the literature are not observed among our species (e.g. wing membrane devoid of scales, Yoshida et al, 1996 ; Gomez et al, 2021 ). However, unlike Gomez et al, 2021 , who studied a large number of transparent species with a wide range of ecologies and belonging to 31 families, our study is restricted to mimetic transparent butterflies and, as such, spans a relatively small number of families.…”

“…To investigate whether transmission properties depend on structural features we used the above measurements of the specular transmittance of transparent patches of each species (see Figure 5—source data 1 for raw spectra) and we calculated the mean transmittance over 300–700 nm, hereafter called mean transmittance, for each spectrum. The physical property 'mean transmittance’ (a proxy for the degree of transparency), is correlated to what is predicted to be perceived by predators based on vision modelling, (see Appendix and Supplementary file 3a–c for details), as shown in Gomez et al, 2021 . Across the 62 species, the mean transmittance ranges from 0.0284 % in Eresia nauplius to 71.7 % in Godyris panthyale (mean: 29.2%, median: 31.6%, Supplementary file 1d ).…”

“…Reducing scale density could also make wings transparent to some extent ( Goodwyn et al, 2009 ). Recently, Gomez et al, 2021 reported that some Lepidoptera achieve transparency with transparent scales. In addition to scale modifications, the presence of nanostructures on the surface of the wing membrane may enhance transparency through the reduction of light reflection, by generating a gradient of refractive index between the chitin-made membrane and the air allowing better penetration of light through the membrane ( Binetti et al, 2009 ; Siddique et al, 2015 ; Yoshida et al, 1997 ).…”

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“…Butterflies, and insects more generally, have evolved transparent wings independently multiple times, often with diverse underlying mechanisms (Dushkina et al, 2017 ; Watson et al, 2017 ). The wings of most butterflies and moths are semi‐translucent when wing scales are removed, but in some cases, there has been selection on transparency to facilitate effective camouflage (Figure 3a , Gomez et al, 2021 ; Johnsen, 2001 ; McClure et al., 2019 ). Many of these wing structures are additionally hydrophobic, another desired characteristic in mask design (El‐Atab et al, 2020 ; Wanasekara & Chalivendra, 2011 ).…”