In mammals, hearing is dependent on three canonical processing stages: (i) an eardrum collecting sound, (ii) a middle ear impedance converter, and (iii) a cochlear frequency analyzer. Here, we show that some insects, such as rainforest katydids, possess equivalent biophysical mechanisms for auditory processing. Although katydid ears are among the smallest in all organisms, these ears perform the crucial stage of air-to-liquid impedance conversion and signal amplification, with the use of a distinct tympanal lever system. Further along the chain of hearing, spectral sound analysis is achieved through dispersive wave propagation across a fluid substrate, as in the mammalian cochlea. Thus, two phylogenetically remote organisms, katydids and mammals, have evolved a series of convergent solutions to common biophysical problems, despite their reliance on very different morphological substrates.

129·kHz (the highest calling note produced by an Arthropod). Paradoxically, these extremely highfrequency sound waves are produced by a low-velocity movement of the stridulatory forewings. Sound production during a wing stroke is pulsed, but the wings do not pause in their closing, requiring that the scraper, in its travel along the file, must do so to create the pulses. We hypothesize that during scraper pauses, the cuticle behind the scraper is bent by the ongoing relative displacement of the wings, storing deformation energy. When the scraper slips free it unbends while being carried along the file and its deformation energy contributes to a more powerful, higher-rate, one-tooth one-wave sound pulse, lasting no more than a few waves at 129·000·Hz. Some other katydid species make pure-tone ultrasonic pulses. Wing velocities and carriers among these pure-tone species fall into two groups: (1) species with ultrasonic carriers below 40·kHz that have higher calling frequencies correlated with higher wing-closing velocities and higher tooth densities: for these katydids the relationship between average tooth strike rate and song frequency approaches 1:1, as in cricket escapement mechanisms; (2) a group of species with ultrasonic carriers above 40·kHz (that includes the Meconematinae): for these katydids closing wing velocities are dramatically lower and they make short trains of pulses, with intervening periods of silence greater than the duration of the pulses they separate. This signal form may be the signature of scraper-stored elastic energy.

Behaviors are challenging to reconstruct for extinct species, particularly the nature and origins of acoustic communication. Here we unravel the song of Archaboilus musicus Gu, Engel and Ren sp. nov., a 165 million year old stridulating katydid. From the exceptionally preserved morphology of its stridulatory apparatus in the forewings and phylogenetic comparison with extant species, we reveal that A. musicus radiated pure-tone (musical) songs using a resonant mechanism tuned at a frequency of 6.4 kHz. Contrary to previous scenarios, musical songs were an early innovation, preceding the broad-bandwidth songs of extant katydids. Providing an accurate insight into paleoacoustic ecology, the low-frequency musical song of A. musicus was well-adapted to communication in the lightly cluttered environment of the mid-Jurassic forest produced by coniferous trees and giant ferns, suggesting that reptilian, amphibian, and mammalian insectivores could have also heard A. musicus' song.call evolution | Tettigoniidae | bushcricket | biomechanics | biological asymmetry K atydids produce species-specific calling songs that form part of the acoustic ecology of tropical forests (1, 2). The rubbing of a toothed vein on one wing against a plectrum on the other wing results in sound production by stridulation, exploiting resonant (musical) (3, 4) or nonresonant (broadband) (4, 5) biophysical mechanisms, depending on the species. Which of these two mechanisms represents ancestral sound production remains a key question in the evolution of insect acoustic communication (6)(7)(8). Here, we reconstruct the song of a katydid fossil with exceptionally well-preserved stridulatory structures, and find that musical singing at low frequencies was already established by the middle Jurassic (165 Ma). We describe this specimen as Archaboilus musicus, from the extinct family Haglidae (Orthoptera), a group basal to all extant katydids (9, 10). These findings imply that A. musicus was nocturnal, and that its call was adapted for long-range communication in an environment with light clutter (11). A recent paleobotanical reconstruction of the geometry, vegetation density, and biomass of the Jurassic Forest from northwest China (12) reveals an environment populated by coniferous trees (e.g., Araucaria) with nearest neighbor distances ranging from 1.5 to 20.3 m, and giant ferns (e.g., Angiopteris, Osmunda, and Caniopteris) occupying the lower layers of the understory forest. This forest architecture indicates a sparse vegetation density that is acoustically compatible with the proposition that the song frequency of A. musicus was well adapted to long-distance communication close to the ground. Such a forested environment would also enable long-range acoustic signaling and communication by other animals (e.g., amphibians, reptilians) as well as a variety of arthropod species (13). Systematic PaleontologyInsecta Linnaeus, 1758; Orthoptera Olivier, 1789; Haglidae Handlirsch, 1906; Cyrtophyllitinae Zeuner, 1935; Archaboilus Martynov, 1937.Archaboilus musicu...

SUMMARYMale field crickets emit pure-tone mating calls by rubbing their wings together. Acoustic radiation is produced by rapid oscillations of the wings, as the right wing (RW), bearing a file, is swept across the plectrum borne on the left wing (LW). Earlier work found the natural resonant frequency (f o ) of individual wings to be different, but there is no consensus on the origin of these differences. Previous studies suggested that the frequency along the song pulse is controlled independently by each wing. It has also been argued that the stridulatory file has a variable f o and that the frequency modulation observed in most species is associated with this variability. To test these two hypotheses, a method was developed for the non-contact measurement of wing vibrations during singing in actively stridulating Gryllus bimaculatus. Using focal microinjection of the neuroactivator eserine into the cricket's brain to elicit stridulation and micro-scanning laser Doppler vibrometry, we monitored wing vibration in actively singing insects. The results show significantly lower f o in LWs compared with RWs, with the LW f o being identical to the sound carrier frequency (N44). But during stridulation, the two wings resonate at one identical frequency, the song carrier frequency, with the LW dominating in amplitude response. These measurements also demonstrate that the stridulatory file is a constant resonator, as no variation was observed in f o along the file during sound radiation. Our findings show that, as they engage in stridulation, cricket wings work as coupled oscillators that together control the mechanical oscillations generating the remarkably pure species-specific song.Supplementary material available online at

SUMMARY To examine whether sound production in katydids relies on an escapement mechanism similar to that of crickets we investigated the functional anatomy and mechanical properties of the stridulatory apparatus in the katydid Panacanthus pallicornis. Males of this species produce sustained pulses with a sharp low frequency peak of ∼5 kHz and a broad band spectrum between 15 and 25 kHz. Simultaneous recordings of movement and sound indicate that the entire stridulatory file is used for sound production and there is nearly a 1:1 correspondence between the number of cycles in a song and the number of teeth on the file. There is an overall tendency for both the spacing of teeth to increase along the file and the velocity of wing closure to increase as the scraper traverses the file. There is considerable variation,however, in the evenness of tooth spacing and in the instantaneous velocity of wing closure during sound production. The production of sustained pulses appears to depend on resonance in the right tegmen, with the left tegmen acting primarily as a damping element. This resonance is not strongly coupled to the scraper and, unlike crickets, the timing of file-scraper interactions,and therefore the phasing of energy input to wing oscillations, is variable. Similarly, the quality of the sound spectrum varies over the course of a single stridulatory wing-stroke. Based on measurements of tooth spacing on the stridulatory file and cycle-by-cycle frequency of sound output, we predicted the velocity of wing movement that would provide consistent phasing of file-scraper interactions with respect to sound-radiating wing oscillations and compared this with measurements of wing velocity. Acceleration of wing velocity during stridulation results in a closer match to the velocity required for optimal phasing during a portion of the call, and this corresponds with higher amplitudes of radiated sound and the excitation of higher order modes of vibration (evident as distinct harmonic peaks in spectrograms). Our results suggest that in katydid stridulation, the movement of the scraper along the file is not regulated by an escapement mechanism as it is in crickets. Instead, katydids that produce pure-tone songs sweep their wings over a range of velocities, within which some portion matches file tooth spacing to give optimal phasing of energy input to excite a resonance in the right tegmen.

Male katydids (Orthoptera: Tettigoniidae) produce mating calls by rubbing the wings together, using specialized structures in their forewings (stridulatory file, scraper and mirror). A large proportion of species (ca. 66%) reported in the literature produces ultrasonic signals as principal output. Relationships among body size, generator structures and the acoustic parameters carrier frequency (fc) and pulse duration (pd), were studied in 58 tropical species that use pure‐tone signals. A comparative analysis, based on the only available katydid phylogeny, shows how changes in sound generator form are related to changes in fc and pd. Anatomical changes of the sound generator that might have been selected via fc and pd are mirror size, file length and number of file teeth. Selection for structures of the stridulatory apparatus that enhance wing mechanics via file‐teeth and scraper morphology was crucial in the evolution of ultrasonic signals in the family Tettigoniidae.

The ear of the bush-cricket, Copiphora gorgonensis, consists of a system of paired eardrums (tympana) on each foreleg. In these insects, the ear is backed by an air-filled tube, the acoustic trachea (AT), which transfers sound from the prothoracic acoustic spiracle to the internal side of the eardrums. Both surfaces of the eardrums of this auditory system are exposed to sound, making it a directionally sensitive pressure difference receiver. A key feature of the AT is its capacity to reduce the velocity of sound propagation and alter the acoustic driving forces at the tympanum. The mechanism responsible for reduction in sound velocity in the AT remains elusive, yet it is deemed to depend on adiabatic or isothermal conditions. To investigate the biophysics of such multiple input ears, we used micro-scanning laser Doppler vibrometry and micro-computed X-ray tomography. We measured the velocity of sound propagation in the AT, the transmission gains across auditory frequencies and the time-resolved mechanical dynamics of the tympanal membranes in C. gorgonensis Tracheal sound transmission generates a gain of approximately 15 dB SPL, and a propagation velocity of ca 255 m s, an approximately 25% reduction from free field propagation. Modelling tracheal acoustic behaviour that accounts for thermal and viscous effects, we conclude that reduction in sound velocity within the AT can be explained, among others, by heat exchange between the sound wave and the tracheal walls.

No abstract