Physical and behavioral adaptations to prevent overheating of the living wings of butterflies.

The wings of Lepidoptera contain a matrix of living cells whose function requires appropriate temperatures. However, given their small thermal capacity, wings can overheat rapidly in the sun. Here we analyze butterfly wings across a wide range of simulated environmental conditions, and find that regions containing living cells are maintained at cooler temperatures. Diverse scale nanostructures and non-uniform cuticle thicknesses create a heterogeneous distribution of radiative cooling that selectively reduces the temperature of structures such as wing veins and androconial organs. These tissues are supplied by circulatory, neural and tracheal systems throughout the adult lifetime, indicating that the insect wing is a dynamic, living structure. Behavioral assays show that butterflies use wings to sense visible and infrared radiation, responding with specialized behaviors to prevent overheating of their wings. Our work highlights the physiological importance of wing temperature and how it is exquisitely regulated by structural and behavioral adaptations.

Tsai CC ，Childers RA ，Nan Shi N ，Ren C ，Pelaez JN ，Bernard GD ，Pierce NE ，Yu N ... -  《Nature Communications》

Air temperature drives the evolution of mid-infrared optical properties of butterfly wings.

This study uncovers a correlation between the mid-infrared emissivity of butterfly wings and the average air temperature of their habitats across the world. Butterflies from cooler climates have a lower mid-infrared emissivity, which limits heat losses to surroundings, and butterflies from warmer climates have a higher mid-infrared emissivity, which enhances radiative cooling. The mid-infrared emissivity showed no correlation with other investigated climatic factors. Phylogenetic independent contrasts analysis indicates the microstructures of butterfly wings may have evolved in part to regulate mid-infrared emissivity as an adaptation to climate, rather than as phylogenetic inertia. Our findings offer new insights into the role of microstructures in thermoregulation and suggest both evolutionary and physical constraints to butterflies' abilities to adapt to climate change.

Krishna A ，Nie X ，Briscoe AD ，Lee J ... -  《Scientific Reports》

Infrared optical and thermal properties of microstructures in butterfly wings.

While surface microstructures of butterfly wings have been extensively studied for their structural coloration or optical properties within the visible spectrum, their properties in infrared wavelengths with potential ties to thermoregulation are relatively unknown. The midinfrared wavelengths of 7.5 to 14 µm are particularly important for radiative heat transfer in the ambient environment, because of the overlap with the atmospheric transmission window. For instance, a high midinfrared emissivity can facilitate surface cooling, whereas a low midinfrared emissivity can minimize heat loss to surroundings. Here we find that the midinfrared emissivity of butterfly wings from warmer climates such as (Oaxaca, Mexico) and (Pichincha, Ecuador) is up to 2 times higher than that of butterfly wings from cooler climates such as (Colorado) and (Florida), using Fourier-transform infrared (FTIR) spectroscopy and infrared thermography. Our optical computations using a unit cell approach reproduce the spectroscopy data and explain how periodic microstructures play a critical role in the midinfrared. The emissivity spectrum governs the temperature of butterfly wings, and we demonstrate that wings heat up to 8 °C more than wings under the same sunlight in the clear sky of Irvine, CA. Furthermore, our thermal computations show that butterfly wings in their respective habitats can maintain a moderate temperature range through a balance of solar absorption and infrared emission. These findings suggest that the surface microstructures of butterfly wings potentially contribute to thermoregulation and provide an insight into butterflies' survival.

Krishna A ，Nie X ，Warren AD ，Llorente-Bousquets JE ，Briscoe AD ，Lee J ... -  《-》

Universal cooling patterns of the butterfly wing scales hierarchy deduced from the heterogeneous thermal and structural properties of Tirumala limniace (Lepidoptera: Nymphalidae, Danainae).

The radiative cooling of butterfly wing scales hierarchy has great value in understanding how poikilotherms adapt to the environment and developing bionic materials. However, it remains unclear what the cooling system is like and how the variation of hierarchy affects the cooling efficiency. Therefore, the correlation between the variations of the structure and emissivity of scale hierarchy is thoroughly investigated in Tirumala limniace (Cramer, 1775), whose thermal properties are highly heterogeneous among different wings and regions but similar between males and females. Patterns were deduced from the biological and model simulation experiments. The scale hierarchy varies at the micro- to nanolevel on both surface and section, corresponding to the variating emissivity. Scales on wing veins and margins have large nanostructured units with small lumens and are distinctly thickened, which bring extraordinarily high emissivity. The variations of light and dark scales, respectively, lead to the high emissivity of the middle region of wings and the front wings. Generally, the elevation of the inner surface area and the thickness of the chitin is the key to enhancing the cooling efficiency. For the first time, the effects of the variation of hierarchy toward emissivity of the mid-infrared spectrum are systematically clarified. It is demonstrated that wing scales integrally differentiate in coping with the heterogeneous cooling needs, which may benefit in balancing multifunctions and the development toward the adaptation to the abiotic environment. The study provides insights into the comprehensive thermoregulation system of butterflies and the further development of radiative cooling materials.

Tang CF ，Li FF ，Cao Y ，Liao HJ ... -  《-》

Structural color in Junonia butterflies evolves by tuning scale lamina thickness.

In diverse organisms, nanostructures that coherently scatter light create structural color, but how such structures are built remains mysterious. We investigate the evolution and genetic regulation of butterfly scale laminae, which are simple photonic nanostructures. In a lineage of buckeye butterflies artificially selected for blue wing color, we found that thickened laminae caused a color shift from brown to blue. Deletion of the patterning gene also altered color via lamina thickening, revealing shared regulation of pigments and lamina thickness. Finally, we show how lamina thickness variation contributes to the color diversity that distinguishes sexes and species throughout the genus . Thus, quantitatively tuning one dimension of scale architecture facilitates both the microevolution and macroevolution of a broad spectrum of hues. Because the lamina is an intrinsic component of typical butterfly scales, our findings suggest that tuning lamina thickness is an available mechanism to create structural color across the Lepidoptera.

Thayer RC ，Allen FI ，Patel NH 《eLife》