The repeated evolution of anti-bat bioacoustics in hawkmoths

Abstract Predator–prey interactions impose strong selective forces, often resulting in remarkable anti-predatory adaptations. Among insects, moths have been engaged in a long-standing arms race with bats, leading to the evolution of diverse anti-predator strategies. Here, we investigate the evolution of anti-bat stridulatory behaviour in hawkmoths (Lepidoptera: Sphingidae) by integrating acoustic recordings, high-resolution scanning electron microscopy and micro-computed tomography imaging and a time-calibrated phylogeny. We classify three distinct ultrasound-producing systems—scale-on-scale, scale-on-spine and scale-on-nodule—based on the interaction of scraper and file components. Building on previous descriptions, we uncover new details of two stridulatory mechanisms and describe for the first time the file component in the scale-on-nodule system of Macroglossinae. Phylogenetic analyses reveal that stridulatory responses to bat echolocation evolved independently multiple times among hawkmoths within the past approximately 30 million years. Furthermore, we demonstrate that divergent lineages produce acoustically distinct signals that correlate with variation in stridulatory morphology and the presence or absence of hearing organs. Collectively, our results highlight the repeated evolution of ultrasonic defences across divergent hawkmoth lineages and underscore predator–prey conflict as a powerful driver of both evolutionary innovation and redundancy in bioacoustic warfare.