Evolution of a Communication System by Sensory Exploitation of Startle Behavior

New communication signals can evolve by sensory exploitation if signaling taps into preexisting sensory biases in receivers [1, 2]. For mate attraction, signals are typically similar to attractive environmental cues like food [3-6], which amplifies their attractiveness to mates, as opposed to aversive stimuli like predator cues. Female field crickets approach the low-frequency calling song of males, whereas they avoid high-frequency sounds like predatory bat calls [7]. In one group of crickets (Eneopterinae: Lebinthini), however, males produce exceptionally high-frequency calling songs in the range of bat calls [8], a surprising signal in the context of mate attraction. We found that female lebinthines, instead of approaching singing males, produce vibrational responses after male calls, and males track the source of vibrations to find females. We also demonstrate that field cricket species closely related to the Lebinthini show an acoustic startle response to high-frequency sounds that generates substrate vibrations similar to those produced by female lebinthine crickets. Therefore, the startle response is the most likely evolutionary origin of the female lebinthine vibrational signal. In field crickets, the brain receives activity from two auditory interneurons; AN1 tuned to male calling song controls positive phonotaxis, and AN2 tuned to high-frequency bat calls triggers negative phonotaxis [9, 10]. In lebinthine crickets, however, we found that auditory ascending neurons are only tuned to high-frequency sounds, and their tuning matches the thresholds for female vibrational signals. Our results demonstrate how sensory exploitation of anti-predator behavior can evolve into a communication system that benefits both senders and receivers.