Sensory systems must change over time to support changing behavioral requirements. Such transformations provide a window for understanding how sensory organs and the underlying neural processing evolve. Praying mantises are the only animals with a single ear in the middle of the body (an auditory cyclops). It exclusively detects ultrasound (30 kHz; above the range of human hearing), and warns the mantis of hunting bats that use ultrasonic sonar. A few mantis species, like Creobroter pictipennis, have evolved a complete, second auditory system. It also has a single ear in the middle of the body (a double cyclops) but detects only 3-5 kHz sound. Comparing species with and without the second ear, this project will study 1) what internal changes lead to the second ear; 2) how the two auditory systems interact; and 3) how these mantises use low-frequency hearing. Synchrotron x-ray imaging will show the progressive anatomical changes that lead to hearing. This technique provides views of internal structures analogous to MRIs, but with 1000 times greater resolution. Laser vibrometry will link minute changes in vibration to the altered anatomy. Neurophysiological and neuroanatomical techniques will determine how the nervous system processes information from each ear. The behaviors requiring a second ear are a puzzle to be addressed by allowing mantises to interact in natural conditions under video and microphone surveillance. Unexpectedly, changes in the respiratory system may be most important in evolving the second, completely independent auditory system. Although previously unknown, sound communication is the probable function of mantis low-frequency hearing. This project brings together for the first time two ultrahigh-resolution techniques to study structure/function changes in the evolution of an auditory system. Over 20 undergraduate research students will receive support to participate in this project.
Our research aims to understand better the transformation from sensory input to behavioral output, and in particular, the evolution of hearing and auditory behaviors. We use as our model system the praying mantis, unique in the world because it has just a single, ‘cyclopean’ ear in the middle of its body. The ear hears ultrasound and is the basis for a highly effective neuro-behavioral system for evading hunting bats. We have also discovered a few mantises that have more recently evolved hearing a second time - there are two cyclopean ears in different parts of the body, two separate auditory systems, two different sound frequency ranges, two different auditory behaviors - an ideal opportunity for studying auditory system evolution (Fig. 1). In the current project we have sought (1) to understand the structure and bioacoustic principles of the second ear compared to the ultrasound ear; (2) to establish whether or not the two auditory systems interact with one another; and (3) to define the acoustic behaviors associated with the new auditory system. We studied the functional anatomy of the second ear with a combination of conventional anatomy, 3D reconstructions from ultra-high resolution CAT scans (Fig. 2), and laser vibrometry that measures tympanum movement. We found that the second ear is built of serially homologous components that nonetheless function in a fundamentally different way from the ultrasound ear. In the latter case, frequency selectivity comes from tympanal structure, but in the newer ear it arises from the neural structures within the ear. Further, the sensitivity of the ultrasound ear arises from a tympanum sandwiched between a deep acoustic chamber and an isolated air sac. The equal level of sensitivity of the newer ear, however, comes from internal pressure within the entire body segment acting on a tympanum without any acoustic chamber. Within the nervous system, we discovered that the second auditory system modulates activity of neurons in the older system. Low-frequency sound occurring at the proper time before ultrasound pulses, reduces the activity of ultrasound-responsive neurons by 50% or more (Fig. 3). This occurs through two neural circuits: a direct path from the second ear to the ultrasound neurons and an indirect path that ascends to the brain and then goes back down to the ultrasound neurons. Auditory information from the second ear travels throughout the entire central nervous system, and does so even faster than information from the older ear that we know controls a high-speed escape system. Despite extensive and repeated efforts, we have not found a discrete, immediate behavior triggered by low-frequency sound. This means that the function of the newer auditory system must be the modulation of the older system to yield different behavioral responses in different behavioral contexts. The function may alternatively or additionally be to modify the internal state of the animal - changing hormone or neuromodulator levels, for instance - in preparation for behavioral demands in the near future. In addition to its intellectual contribution to understanding auditory processing and the evolution of sensory systems, the broader impact of our work is the research training of undergraduates. Students have played crucial roles in all aspects of the research, each one working on their own individual project. With the support of the grant, 23 undergraduates have trained, or are currently training in the lab, and most have had intensive summer internships. The number includes 11 women and five minority students. Of the 18 students who have graduated, nine have been authors on presentations at national professional meetings (seven presenting in person), and three are authors on manuscripts for publication. The career trajectories of the graduates include about a third who have gone to medical school. However, the best measure of long-term career impact is the eight students who have gone on to Ph.D. programs in neuroscience or related fields as their next step toward becoming research scientists themselves.
