Adaptive shifts underlie the divergence in wing morphology in bombycoid moths

Abstract

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

“…For example, robotic flapping-wing micro air vehicles (FW-MAVs) have greater power efficiency and control than fixed-wing and rotary-wing aircraft of similar size [4,5]. Since the origin of flapping flight in insects, a wide diversity of wing morphologies (size, shape and mechanics), movements and flight behaviours have evolved [6][7][8][9]. A central question in the evolution of flapping flight is whether divergent strategies (combinations of wing shape, size and kinematics) arise to achieve similar flight performance.…”

“…Hawkmoths (Sphingidae) and wild silk moths (Saturniidae) are diverse sister clades separated by approximately 60 Ma of evolution [9,16,17]. We recently showed that wing shape and size diverges between the families through an adaptive shift [9] coincident with the inter-familial divergence in life history [18][19][20] and flight behaviour [18][19][20].…”

“…Hawkmoths (Sphingidae) and wild silk moths (Saturniidae) are diverse sister clades separated by approximately 60 Ma of evolution [9,16,17]. We recently showed that wing shape and size diverges between the families through an adaptive shift [9] coincident with the inter-familial divergence in life history [18][19][20] and flight behaviour [18][19][20]. However, wing morphology diverged between the clades in a way that belies simple intuition about how shape should affect performance based on the behavioural demands of each family [9].…”

“…We recently showed that wing shape and size diverges between the families through an adaptive shift [9] coincident with the inter-familial divergence in life history [18][19][20] and flight behaviour [18][19][20]. However, wing morphology diverged between the clades in a way that belies simple intuition about how shape should affect performance based on the behavioural demands of each family [9]. Hawkmoths are active, fast fliers [20], well known for their ability to sustain long-duration bouts of hover [21][22][23][24], where some species can track flower oscillations up to frequencies of 14 Hz [24,25].…”

“…Hawkmoths are active, fast fliers [20], well known for their ability to sustain long-duration bouts of hover [21][22][23][24], where some species can track flower oscillations up to frequencies of 14 Hz [24,25]. Yet, hawkmoths evolved small wings of high aspect ratio (AR), non-dimensional radius of the second moment of area (r 2 ) and wing loading (W s ), metrics typically associated with power reduction and a high lift-to-drag ratio [9,26]. These metrics are also associated with poor manoeuvrability in fixed-wing aircraft, although animal fliers partially control flight more like rotary-blade systems where force vectors are modulated by wing rotations [27,28].…”