Enhanced flight performance and adaptive evolution of Mesozoic giant cicadas

Abstract

Insects have evolved diverse ecological flight behaviors and adaptations that played a key role in their large-scale evolutionary patterns. However, the evolution of their flight performance is poorly understood because reconstructing flight abilities of extinct insects is highly challenging. Here, we propose an integrated approach to reveal the evolution of flight performance of Palaeontinidae (giant cicadas), a Mesozoic arboreal insect clade with large bodies and wings. Our analyses unveil a faunal turnover from early to late Palaeontinidae during the latest Jurassic–earliest Cretaceous, accompanied by a morphological adaptive shift and remarkable improvement in flight abilities including increased flight speed and enhanced maneuverability. The adaptive aerodynamic evolution of Palaeontinidae may have been stimulated by the rise of early birds, supporting the hypothesis of an aerial evolutionary arms race (Air Race) between Palaeontinidae and birds. Our results provide a potential example of predator-induced morphological and behavioral macroevolution and contribute to our understanding of how powered flight has shaped animal evolution.