Multispecies comparisons support a startle response origin for a novel vibrational signal in the cricket tribe Lebinthini

Many animals communicate using call and response signals, but the evolutionary origins of this type of communication are largely unknown. In most cricket species, males sing and females walk or fly to calling males. In the tribe Lebinthini, however, males produce calls that trigger a vibrational reply from females, and males use the substrate vibrations to find the responding female. Here we assess two hypotheses regarding the behavioral origin of this multimodal duet in the Lebinthini. We conducted playback experiments and measured behavioral and neuronal responses in multiple related cricket species to assess whether the precursor to the lebinthine duet was 1) a startle response to high-frequency sound, or 2) elaboration of a preexisting courtship behavior. We found behavioral similarities between the vibrational response of Lebinthini females and the acoustic startle behavior in other gryllid crickets. Specifically, the amplitude of the vibrational reply increases with male song amplitude in Lebinthini, and the magnitude of vibrations produced by two gryllid species when startled with ultrasound also correlates with the stimulus amplitude. Like in-flight startle behavior, the startle vibrations produced by perched crickets are suppressed when low-frequency sound is played simultaneously. We also observed courtship behavior in four gryllid species and found few instances of female vibration. Vibrational signals observed in Gryllus pennsylvanicus females were not correlated with male calls and occurred more frequently in pairs that did not mate after courtship. Combined, accumulating evidence supports the hypothesis that the lebinthine duet more likely evolved from a startle precursor than courtship behavior.