Mechanosensory cephalic bristles mediate rapid flight initiation in endothermic hawkmoths

AbstractEndothermic 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 a considerable risk if they need to rapidly escape from predators. Here, we show that upon experiencing a sudden air-puff on the head, hawkmoths rapidly initiate flight bypassing the pre-flight shivering phase. This response is mediated by mechanosensory cephalic bristles that are buried under the scales on their head. Cephalic bristle mediated flight entails a stereotypic triggering of various flight-related reflexes including antennal positioning, foreleg extension, wing movement, and abdominal flexion. Some mechanosensory neurons underlying cephalic bristles arborize in the subesophageal zone (SEZ) and antennal motor and mechanonsensory center (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 wing motion following cephalic bristle-stimulation occurs at lower thoracic temperatures than required for voluntary flight. Electromyogram recordings from steering and indirect flight muscles show significant variability in activation latency in response to cephalic bristle stimulus. The range of latency values among different muscles overlaps, suggesting that cephalic bristle stimulation activates steering muscles, thereby generating high-amplitude wing movement at lower thoracic temperatures. Concomitant activation of the indirect flight muscles initiates thoracic warm-up in preparation for longer flight. Thus, akin to locusts, the cephalic bristle system in hawkmoths rapidly triggers flight upon sensing danger, ensuring swift escape from potential threats.