Autonomous Expansion of Grasshopper Wings Reveals External Forces Contribute to Final Adult Wing Shape.

Abstract

Ecdysis, transformation from juvenile to adult form in insects, is time-consuming and leaves insects vulnerable to predation. For winged insects, the process of wing expansion during ecdysis, unfurling and expanding the wings, is a critical bottleneck in achieving sexual maturity. Internal and external forces play a role in wing expansion. Vigorous abdominal pumping during wing expansion allows insects to pressurize and inflate their wings, filling them with hemolymph. In addition, many insects adopt expansion-specific postures and, if inhibited, do not expand their wings normally, suggesting that external forces such as gravity may play a role. However, two previous studies over 40years ago, reported that the forewings of swarming locusts can expand autonomously when removed from the emerging insect and laid flat on a saline solution. Termed "autoexpansion," we replicated previous experiments of autoexpansion on flat liquid media, documenting changes in both wing length and area over time while also focusing on the role of gravity in autoexpansion. Using the North American bird grasshopper Schistocerca americana, we tested four autoexpansion treatments of varying surface tension and hydrophobicity (gravity, deionized water, buffer, and mineral oil) while simultaneously observing and measuring intact, normal wing expansion. Finally, we constructed a simple model of a viscoelastic expanding wing subjected to gravity, to determine whether it could capture aspects of wing expansion. Our data confirmed that wing autoexpansion does occur in S. americana, but autoexpanding wings, especially hindwings, failed to increase to the same final length and area as intact wings. We found that gravity plays an important role in wing expansion, early in the expansion process. Combined with the significant mass increase we documented in intact wings, it suggests that hydraulic pumping of hemolymph into the wings plays an important role in increasing the area of expanding wings, especially in driving expansion of the large, pleated hindwings. Autoexpansion in a non-swarming orthopteran suggests that local cues driving wing autoexpansion may serve a broader purpose, reducing total expansion time and costs by shifting some processes from central to local control. Documenting wing autoexpansion in a widely studied model organism and demonstrating a mathematical model provides a tractable new system for exploring higher level questions about the mechanisms of wing expansion and the implications of autoexpansion, as well as potential bioinspiration for future technologies applicable to micro-air vehicles, space exploration, or medical and prosthetic devices.