Thorin Jonsson

Convergent Evolution Between Insect and Mammalian Audition

How to Hear In mammalian ears, a chain of biophysical events allows for the translation of airborne acoustic energy into mechanical vibrations that can be detected by mechanosensory cells in the cochlear. Mammalian ears have been considered largely unique in this transformation because it is the delicate, mammalian-specific, bones of the middle ear that facilitate this transmission, known as impedence conversion. In most other vertebrates the bones that make up the middle ear function as part of the lower jaw, limiting the potential for vertebrate convergence in this process. However, Montealegre-Z. et al. (p. 968, see the Perspective by Hoy) show that the rainforest katydid, an insect with ears on its hind legs, have converged on a similar three step impedence conversion process using a unique tympanum-lever organ. This convergence, across millions of years of evolutionary distance, shows the flexibility of morphology to adapt to biophysical challenges. In an example of convergent evolution, rainforest katydids hear using similar mechanisms to those found in mammalian ears. 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.

Sound radiation and wing mechanics in stridulating field crickets (Orthoptera: Gryllidae)

SUMMARY Male 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 (fo) 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 fo 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 crickets brain to elicit stridulation and micro-scanning laser Doppler vibrometry, we monitored wing vibration in actively singing insects. The results show significantly lower fo in LWs compared with RWs, with the LW fo 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 fo 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.

Sound production during agonistic behavior of male Drosophila melanogaster

Male Drosophila fruitflies acquire and defend territories in order to attract females for reproduction. Both, male-directed agonistic behavior and female-directed courtship consist of series of recurrent stereotypical components. Various studies demonstrated the importance of species-specific sound patterns generated by wing vibration as being critical for male courtship success. In this study we analyzed the patterns and importance of sound signals generated during agonistic interactions of male Drosophila melanogaster. In contrast to acoustic courtship signals that consist of sine and pulse patterns and are generated by one extended wing, agonistic signals lack sine-like components and are generally produced by simultaneous movements of both wings. Though intra-pulse oscillation frequencies (carrier frequency) are identical, inter-pulse intervals are twice as long and more variable in aggression signals than in courtship songs, where their precise temporal pattern serves species recognition. Acoustic signals accompany male agonistic interactions over their entire course but occur particularly often after tapping behavior which is a major way to identify the gender of the interaction partner. Since similar wing movements may either be silent or generate sound and wing movements with sound have a greater impact on the subsequent behavior of a receiver, sound producing wing movements seem to be generated intentionally to serve as a specific signal during fruit fly agonistic encounters.

Ultrasonic reverse stridulation in the spider-like katydid Arachnoscelis (Orthoptera: Listrosceledinae)

This paper illustrates the biomechanics of sound production in the neotropical predaceous katydid Arachnoscelis arachnoides (Insecta: Orthoptera: Tettigoniidae). Described and previously known from only one male specimen, this genus of predaceous katydids resembles spiders in their general body appearance. To call distant females, male katydids produce songs by stridulation where one forewing possessing a sclerotized file rubs against a row of teeth (scraper) on the other wing. In most katydid species, the songs are produced during the wing-closing phase of the stridulation. Morphological comparative studies of the stridulatory apparatus of the type specimen of Arachnoscelis arachnoides and males of other closely related species suggest that this insect sings with a frequency of ca. 80 kHz to attract conspecific females. We found an abundant population of A. arachnoides in Central Northeast of Colombia and undertook a complete analysis of the biomechanics of stridulation in this species. Using ultrasound-sensitive equipment and high-speed video, we determined that male A. arachnoides sing at ca. 74 kHz and use elastic energy and wing deformation to reach such ultrasonic frequencies. In contrast to most katydids, males of this species produce their calls during the opening phase of the wing; this form of stridulation is discussed.

Chamber music - An unusual Helmholtz resonator for song amplification in a Neotropical bush-cricket (Orthoptera, Tettigoniidae).

ABSTRACT Animals use sound for communication, with high-amplitude signals being selected for attracting mates or deterring rivals. High amplitudes are attained by employing primary resonators in sound-producing structures to amplify the signal (e.g. avian syrinx). Some species actively exploit acoustic properties of natural structures to enhance signal transmission by using these as secondary resonators (e.g. tree-hole frogs). Male bush-crickets produce sound by tegminal stridulation and often use specialised wing areas as primary resonators. Interestingly, Acanthacara acuta, a Neotropical bush-cricket, exhibits an unusual pronotal inflation, forming a chamber covering the wings. It has been suggested that such pronotal chambers enhance amplitude and tuning of the signal by constituting a (secondary) Helmholtz resonator. If true, the intact system – when stimulated sympathetically with broadband sound – should show clear resonance around the song carrier frequency which should be largely independent of pronotum material, and change when the system is destroyed. Using laser Doppler vibrometry on living and preserved specimens, microcomputed tomography, 3D-printed models and finite element modelling, we show that the pronotal chamber not only functions as a Helmholtz resonator owing to its intact morphology but also resonates at frequencies of the calling song on itself, making song production a three-resonator system. Summary: Laser vibrometry, microcomputed tomography and finite element modelling are used to show that an unusual pronotal inflation covering the wings of a bush-cricket acts as a Helmholtz resonator.

Auditory sensitivity, spatial dynamics, and amplitude of courtship song in Drosophila melanogaster

Acoustic communication is an important component of courtship in Drosophila melanogaster. It takes the form of courtship song produced by males through the unilateral extension and vibration of a wing. Following the paradigm of sender-receiver matching, song content is assumed to match tuning in the auditory system, however, D. melanogaster audition is nonlinear and tuning dependent upon signal amplitude. At low stimulus amplitudes or in the absence of sound the antenna is tuned into song frequency, but as amplitude increases the antennas resonance is shifted up by hundreds of Hertz. Accurate measurements of song amplitude have been elusive because of the strong dependency of amplitude upon the spatial geometry between sender and receiver. Here, D. melanogaster auditory directional sensitivity and the geometric position between the courting flies are quantified. It is shown that singing occurs primarily from positions resulting in direct stimulation of the female antenna. Using this information, it is established that the majority of song is louder than theoretically predicted and at these sound levels the female antenna should not amplify or be tuned into song. The study implies that Drosophila hearing, and, in particular, its active mechanisms, could function in a broader context than previously surmised.

Microacoustics: maintaining an ecologically relevant scale in insect bioacoustics

A major challenge when studying an organism is to maintain its environment and context as reliably as possible. When looking at sensory systems it is crucial not to assume the animals perception the same as ours and instead measure and mimic more accurately the natural stimuli driving the sensors. In insect bioacoustics the usual practice in playback and recording techniques overlooks differences in scale and context in which the organisms sensory system evolved. Here we present an approach to emit and record low‐amplitude near‐field sound, while maintaining an ecologically relevant scale, in Drosophila melanogaster. To mimic the effect of male courtship song on the female sound receiver (antennae) a mechanical microwing was constructed simulating, in power and geometry, particle velocity signals emitted by singing males, with its efficacy tested by behavioural assay. Development of a miniature particle velocitymicrophone was also initiated for recording signals in the flys immediate vicinity (<2 mm) to elucidate the magnitude, temporal and radiation characteristics of the produced sound‐field.