Adaptive shifts underlie the divergence in wing morphology in bombycoid moths.

The evolution of flapping flight is linked to the prolific success of insects. Across Insecta, wing morphology diversified, strongly impacting aerodynamic performance. In the presence of ecological opportunity, discrete adaptive shifts and early bursts are two processes hypothesized to give rise to exceptional morphological diversification. Here, we use the sister-families Sphingidae and Saturniidae to answer how the evolution of aerodynamically important traits is linked to clade divergence and through what process(es) these traits evolve. Many agile Sphingidae evolved hover feeding behaviours, while adult Saturniidae lack functional mouth parts and rely on a fixed energy budget as adults. We find that Sphingidae underwent an adaptive shift in wing morphology coincident with life history and behaviour divergence, evolving small high aspect ratio wings advantageous for power reduction that can be moved at high frequencies, beneficial for flight control. By contrast, Saturniidae, which do not feed as adults, evolved large wings and morphology which surprisingly does not reduce aerodynamic power, but could contribute to their erratic flight behaviour, aiding in predator avoidance. We suggest that after the evolution of flapping flight, diversification of wing morphology can be potentiated by adaptative shifts, shaping the diversity of wing morphology across insects.

The evolution of two distinct strategies of moth flight.

Across insects, wing shape and size have undergone dramatic divergence even in closely related sister groups. However, we do not know how morphology changes in tandem with kinematics to support body weight within available power and how the specific force production patterns are linked to differences in behaviour. Hawkmoths and wild silkmoths are diverse sister families with divergent wing morphology. Using three-dimensional kinematics and quasi-steady aerodynamic modelling, we compare the aerodynamics and the contributions of wing shape, size and kinematics in 10 moth species. We find that wing movement also diverges between the clades and underlies two distinct strategies for flight. Hawkmoths use wing kinematics, especially high frequencies, to enhance force and wing morphologies that reduce power. Silkmoths use wing morphology to enhance force, and slow, high-amplitude wingstrokes to reduce power. Both strategies converge on similar aerodynamic power and can support similar body weight ranges. However, inter-clade within-wingstroke force profiles are quite different and linked to the hovering flight of hawkmoths and the bobbing flight of silkmoths. These two moth groups fly more like other, distantly related insects than they do each other, demonstrating the diversity of flapping flight evolution and a rich bioinspired design space for robotic flappers.