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

• Published in: Nature communications Vol. 11; no. 1; pp. 551 - 14
• Main Authors: Tsai, Cheng-Chia, Childers, Richard A., Nan Shi, Norman, Ren, Crystal, Pelaez, Julianne N., Bernard, Gary D., Pierce, Naomi E., Yu, Nanfang
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 28.01.2020; Nature Publishing Group; Nature Portfolio
• Subjects: 14/34; 140/125; 147/135; 147/28; 631/158/856; 631/57/1464; 631/601/1466; 631/601/18; 639/766/747; Adaptation; Adaptation, Physiological - physiology; Animals; BASIC BIOLOGICAL SCIENCES; Behavior; Behavior, Animal; Butterflies & moths; Butterflies - physiology; Cells (biology); Energy Metabolism - physiology; Environmental conditions; Hemolymph - physiology; Humanities and Social Sciences; Infrared radiation; Infrared Rays; Insects; Models, Biological; multidisciplinary; Nanostructure; Nanostructures; Organs; Overheating; Radiation; Science; Science (multidisciplinary); Solar Energy; Specific heat; Temperature; Thermal capacity; Thermodynamics; Thermosensing; Thermotolerance - physiology; Wings; Wings, Animal - anatomy & histology; Wings, Animal - cytology; Wings, Animal - physiology; Wings, Animal - radiation effects
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-14408-8

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. Butterfly wings have low thermal capacity and thus are vulnerable to damage by overheating. Here, Tsai et al. take an interdisciplinary approach to reveal the organs, nanostructures and behaviors that enable butterflies to sense and regulate their wing temperature.