Mechanosensory cephalic bristles mediate rapid flight initiation in hawkmoths

Endothermic insects including bees, butterflies, and moths need to warm up their flight muscles before taking flight. For instance, diurnal butterflies bask in the sun to heat their flight muscles, whereas nocturnal hawkmoths display a pre-flight shivering behavior in which small-amplitude wing movements cause flight muscles to warm up, eventually generating large-amplitude wing motion for flight. The time required for warm-up puts such insects at considerable risk if they need to rapidly escape from predators. Here, we show that upon experiencing a sudden air-puff on the head, hawkmoths with lower thoracic temperatures can rapidly initiate flight without the need for pre-flight shivering. This response is mediated by mechanosensory cephalic bristles that are located beneath the scales on their head. When activated, these bristles trigger a set of flight-related reflexes including antennal positioning, foreleg extension, wing movement, and abdominal flexion. Some of the mechanosensory neurons associated with the cephalic bristles arborize in the subesophageal zone (SEZ) and antennal motor and mechanonsensory centre (AMMC), whereas most arborize in pro-, meso- and meta-thoracic ganglia, which contain the motor circuitry for foreleg motion, flight, and abdominal flexion. Thermal recordings revealed that large-amplitude flapping following cephalic bristle-stimulation occurs at lower thoracic temperatures than required for endogenously-initiated take off. Electromyogram recordings from steering and indirect flight muscles show significant variability in activation latency in response to cephalic bristle stimuli. The range of latency values among different muscles overlaps, suggesting that cephalic bristle stimulation broadly activates indirect flight and steering muscles, thereby generating high-amplitude wing movement at lower thoracic temperatures. Thus, akin to locusts, the cephalic bristle system in hawkmoths rapidly triggers flight upon sensing danger, ensuring swift escape from potential threats.