In different insect taxa, ears can be found on virtually any part of the body. Comparative anatomy and similarities in the embryological development of ears in divergent taxa suggest that they have evolved multiple times from ubiquitous stretch or vibration receptors, but the homology of these structures has not yet been rigorously tested. Here we provide detailed analysis of a novel set of hearing organs in a relatively "primitive" atympanate bladder grasshopper (Bullacris membracioides) that is capable of signaling acoustically over 2 km. We use morphological, physiological, and behavioral experiments to demonstrate that this species has six pairs of serially repeated abdominal ears derived from proprioceptive pleural chordotonal organs (plCOs). We demonstrate continuity in auditory function from the five posterior pairs, which are simple forms comprising 11 sensilla and resembling plCOs in other grasshoppers, to the more complex anterior pair, which contains 2000 sensilla and is homologous to the single pair of tympanate ears found in "modern" grasshoppers. All 12 ears are morphologically differentiated, responsive to airborne sound at frequencies and intensities that are biologically significant (tuned to 1.5 and 4 kHz; 60-98 dB SPL), and capable of mediating behavioral responses of prospective mates. These data provide evidence for the transition in function and selective advantage that must occur during evolutionary development of relatively complex organs from simpler precursors. Our results suggest that ancestral insects with simple atympanate pleural receptors may have had hearing ranges that equal or exceed those of contemporary insects with complex tympanal ears. Moreover, auditory capability may be more prevalent among modern insect taxa than the presence of overt tympana indicates.
Copyright 2003 Wiley-Liss, Inc.