An auditory bicyclops: Two-eared mantises

Most praying mantises detect ultrasound at 30-50 kHz using a single, ‘cyclopean’ ear in the ventral midline of the metathorax. This auditory system evolved once 115-120 mya. Ultrasonic hearing provides very effective protection from bat predation by triggering a complex evasive behavior. At least seven mantis lineages have broadened their auditory capabilities by evolving a second, serially homologous, cyclopean auditory system in the mesothorax. It hears only 2-4 kHz sounds and has sensitivity equal to or greater than the high-frequency (HF) system. Although similar in overall design, the mesothoracic ear lacks the auditory chamber that is a prominent feature of the HF ear. The two mesothoracic tympana have an unusual, groove-like shape. A neurophysiological timing map shows that low-frequency (LF) auditory activity travels throughout the entire CNS and does so almost as quickly as the HF activity. Each auditory system has its own interneurons and may function independently. However, under specific stimulus conditions, the LF system can reduce activity in some HF interneurons, and increase the activity of others. Despite intensive testing, we have found no behavior directly elicited by LF sound in contexts including intraspecific communication, prey detection, or predator avoidance. We propose that LF sounds change the internal state of the animal in preparation for later behavioral requirements. For instance, a decision to stay or leave a perch might be based on presence or absence of singing prey. The independent evolution of mesothoracic, LF hearing in so many lineages suggests that it serves an important function, that the ventral midline is the preferred location for ears in mantises, and that for insects, auditory systems are easy to build.