Dipteran wing damage discriminates between flight motor inertial-elastic distributions

Abstract

Insects frequently experience irreversible wing damage, yet many maintain flight by adjusting their wingbeat. In Diptera, wingbeat frequency generally increases as wing inertia is lost, but considerably less than predicted by classical models of the flight motor. In this work, we use an inverse-problem approach to identify passive mechanical features of the dipteran flight motor that explain this discrepancy and reproduce experimentally-observed frequency scaling. Combining spatially resolved reconstruction of wing inertia and motor elasticity, finite-element analysis of thoracic deformation, and data-driven viscoelastic models of asynchronous flight muscle, we identify that a compounding interaction between wing root flexion, wing aerodynamics, and muscular viscoelasticity explain the depressed scaling of wingbeat frequency with loss of inertia. Wing inertia is strongly non-uniform and dominated by the vein structure, leading to further depression with respect to loss of area. But, by contrast, thoracic effective inertia is negligible across a wide array of Dipterans and does not contribute to damage-related scaling. Together these results indicate that much of the dipteran flight motor's responses to wing damage can emerge passively from interactions between the wing, thorax, and muscles; and suggest that a hybrid-elastic architecture with a compliant wing root may be widespread across Diptera. More broadly, we identify wing damage as a tool that can quantitatively discriminate between different candidate models of the insect flight motor, and suggest that altered motor operating conditions can identify mechanical properties difficult to infer from intact flight alone.