Natasha Mhatre

A Tympanal Insect Ear Exploits a Critical Oscillator for Active Amplification and Tuning

Summary A dominant theme of acoustic communication is the partitioning of acoustic space into exclusive, species-specific niches to enable efficient information transfer. In insects, acoustic niche partitioning is achieved through auditory frequency filtering, brought about by the mechanical properties of their ears [1]. The tuning of the antennal ears of mosquitoes [2] and flies [3], however, arises from active amplification, a process similar to that at work in the mammalian cochlea [4]. Yet, the presence of active amplification in the other type of insect ears—tympanal ears—has remained uncertain [5]. Here we demonstrate the presence of active amplification and adaptive tuning in the tympanal ear of a phylogenetically basal insect, a tree cricket. We also show that the tree cricket exploits critical oscillator-like mechanics, enabling high auditory sensitivity and tuning to conspecific songs. These findings imply that sophisticated auditory mechanisms may have appeared even earlier in the evolution of hearing and acoustic communication than currently appreciated. Our findings also raise the possibility that frequency discrimination and directional hearing in tympanal systems may rely on physiological nonlinearities, in addition to mechanical properties, effectively lifting some of the physical constraints placed on insects by their small size [6] and prompting an extensive reexamination of invertebrate audition.

Changing resonator geometry to boost sound power decouples size and song frequency in a small insect

Despite their small size, some insects, such as crickets, can produce high amplitude mating songs by rubbing their wings together. By exploiting structural resonance for sound radiation, crickets broadcast species-specific songs at a sharply tuned frequency. Such songs enhance the range of signal transmission, contain information about the signaler’s quality, and allow mate choice. The production of pure tones requires elaborate structural mechanisms that control and sustain resonance at the species-specific frequency. Tree crickets differ sharply from this scheme. Although they use a resonant system to produce sound, tree crickets can produce high amplitude songs at different frequencies, varying by as much as an octave. Based on an investigation of the driving mechanism and the resonant system, using laser Doppler vibrometry and finite element modeling, we show that it is the distinctive geometry of the crickets’ forewings (the resonant system) that is responsible for their capacity to vary frequency. The long, enlarged wings enable the production of high amplitude songs; however, as a mechanical consequence of the high aspect ratio, the resonant structures have multiple resonant modes that are similar in frequency. The drive produced by the singing apparatus cannot, therefore, be locked to a single frequency, and different resonant modes can easily be engaged, allowing individual males to vary the carrier frequency of their songs. Such flexibility in sound production, decoupling body size and song frequency, has important implications for conventional views of mate choice, and offers inspiration for the design of miniature, multifrequency, resonant acoustic radiators.

Matching sender and receiver: poikilothermy and frequency tuning in a tree cricket

SUMMARY Animals communicate in non-ideal and noisy conditions. The primary method they use to improve communication efficiency is sender-receiver matching: the receivers sensory mechanism filters the impinging signal based on the expected signal. In the context of acoustic communication in crickets, such a match is made in the frequency domain. The males broadcast a mate attraction signal, the calling song, in a narrow frequency band centred on the carrier frequency (CF), and the females are most sensitive to sound close to this frequency. In tree crickets, however, the CF changes with temperature. The mechanisms used by female tree crickets to accommodate this change in CF were investigated at the behavioural and biomechanical level. At the behavioural level, female tree crickets were broadly tuned and responded equally to CFs produced within the naturally occurring range of temperatures (18 to 27°C). To allow such a broad response, however, the transduction mechanisms that convert sound into mechanical and then neural signals must also have a broad response. The tympana of the female tree crickets exhibited a frequency response that was even broader than suggested by the behaviour. Their tympana vibrate with equal amplitude to frequencies spanning nearly an order of magnitude. Such a flat frequency response is unusual in biological systems and cannot be modelled as a simple mechanical system. This feature of the tree cricket auditory system not only has interesting implications for mate choice and species isolation but may also prove exciting for bio-mimetic applications such as the design of miniature low frequency microphones.

Mechanical response of the tympanal membranes of the tree cricket Oecanthus henryi

Crickets have two tympanal membranes on the tibiae of each foreleg. Among several field cricket species of the genus Gryllus (Gryllinae), the posterior tympanal membrane (PTM) is significantly larger than the anterior membrane (ATM). Laser Doppler vibrometric measurements have shown that the smaller ATM does not respond as much as the PTM to sound. Hence the PTM has been suggested to be the principal tympanal acoustic input to the auditory organ. In tree crickets (Oecanthinae), the ATM is slightly larger than the PTM. Both membranes are structurally complex, presenting a series of transverse folds on their surface, which are more pronounced on the ATM than on the PTM. The mechanical response of both membranes to acoustic stimulation was investigated using microscanning laser Doppler vibrometry. Only a small portion of the membrane surface deflects in response to sound. Both membranes exhibit similar frequency responses, and move out of phase with each other, producing compressions and rarefactions of the tracheal volume backing the tympanum. Therefore, unlike field crickets, tree crickets may have four instead of two functional tympanal membranes. This is interesting in the context of the outstanding question of the role of spiracular inputs in the auditory system of tree crickets.

Male spacing behaviour and acoustic interactions in a field cricket: implications for female mate choice

Males of several acoustically communicating orthopteran species form spatially and temporally structured choruses. We investigated whether male field crickets of the species Plebeiogryllus guttiventris formed choruses in the field. Males formed spatial aggregations and showed fidelity to a calling site within a night, forming stable choruses. Within aggregations, the acoustic ranges of males overlapped considerably. We tested whether males within hearing range of each other interacted acoustically. The chirps of simultaneously calling males were aphasic with respect to each other and showed no significant alternation or synchrony of calls. Some individuals changed temporal features of their calling songs such as chirp durations and chirp rates in response to a simultaneously calling neighbour. The implications of these results for female mate choice are discussed.

Phonotactic walking paths of field crickets in closed-loop conditions and their simulation using a stochastic model.

SUMMARY Field cricket females localize one of many singing males in the field in closed-loop multi-source conditions. To understand this behaviour, field cricket phonotaxis was investigated in a closed-loop walking phonotaxis paradigm, in response to two simultaneously active speakers playing aphasic calling songs. Female phonotactic paths were oriented towards the louder sound sources, but showed great inter-individual variability. Decisions made in the initial phases were correlated with the overall directions of the paths. Interestingly, the sound pressure levels of stimuli did not greatly influence several features of phonotactic paths such as sinuosity, walking bout lengths and durations. In order to ascertain the extent of our understanding of walking phonotaxis, a stochastic model was used to simulate the behaviour observed in the experiment. The model incorporated data from the experiment and our current understanding of field cricket auditory physiology. This model, based on stochastic turning towards the louder side, successfully recaptured several qualitative and quantitative features of the observed phonotactic paths. The simulation also reproduced the paths observed in a separate outdoor field experiment. Virtual crickets that were unilaterally deafened or had poor ear directionality exhibited walking paths similar to those observed in previous experiments.

Predicting acoustic orientation in complex real-world environments.

SUMMARY Animals have to accomplish several tasks in their lifetime, such as finding food and mates and avoiding predators. Animals that locate these using sound need to detect, recognize and localize appropriate acoustic objects in their environment, typically in noisy, non-ideal conditions. Quantitative models attempting to explain or predict animal behaviour should be able to accurately simulate behaviour in such complex, real-world conditions. Female crickets locate potential mates in choruses of simultaneously calling males. In the present study, we have tested field cricket acoustic orientation behaviour in complex acoustic conditions in the field and also successfully predicted female orientation and paths under these conditions using a simulation model based on auditory physiology. Such simulation models can provide powerful tools to predict and dissect patterns of behaviour in complex, natural environments.

Energy localization and frequency analysis in the locust ear.

Animal ears are exquisitely adapted to capture sound energy and perform signal analysis. Studying the ear of the locust, we show how frequency signal analysis can be performed solely by using the structural features of the tympanum. Incident sound waves generate mechanical vibrational waves that travel across the tympanum. These waves shoal in a tsunami-like fashion, resulting in energy localization that focuses vibrations onto the mechanosensory neurons in a frequency-dependent manner. Using finite element analysis, we demonstrate that two mechanical properties of the locust tympanum, distributed thickness and tension, are necessary and sufficient to generate frequency-dependent energy localization.

Enhanced functional and structural domain assignments using remote similarity detection procedures for proteins encoded in the genome of Mycobacterium tuberculosis H37Rv

The sequencing of theMycobacterium tuberculosis (MTB) H37Rv genome has facilitated deeper insights into the biology of MTB, yet the functions of many MTB proteins are unknown. We have used sensitive profile-based search procedures to assign functional and structural domains to infer functions of gene products encoded in MTB. These domain assignments have been made using a compendium of sequence and structural domain families. Functions are predicted for 78% of the encoded gene products. For 69% of these, functions can be inferred by domain assignments. The functions for the rest are deduced from their homology to proteins of known function. Superfamily relationships between families of unknown and known structures have increased structural information by ∼ 11%. Remote similarity detection methods have enabled domain assignments for 1325 ‘hypothetical proteins’. The most populated families in MTB are involved in lipid metabolism, entry and survival of the bacillus in host. Interestingly, for 353 proteins, which we refer to as MTB-specific, no homologues have been identified. Numerous, previously unannotated, hypothetical proteins have been assigned domains and some of these could perhaps be the possible chemotherapeutic targets. MTB-specific proteins might include factors responsible for virulence. Importantly, these assignments could be valuable for experimental endeavors. The detailed results are publicly available at http://hodgkin.mbu.iisc.ernet.in/∼dots.

Tree crickets optimize the acoustics of baffles to exaggerate their mate-attraction signal

Object manufacture in insects is typically inherited, and believed to be highly stereotyped. Optimization, the ability to select the functionally best material and modify it appropriately for a specific function, implies flexibility and is usually thought to be incompatible with inherited behaviour. Here, we show that tree-crickets optimize acoustic baffles, objects that are used to increase the effective loudness of mate-attraction calls. We quantified the acoustic efficiency of all baffles within the naturally feasible design space using finite-element modelling and found that design affects efficiency significantly. We tested the baffle-making behaviour of tree crickets in a series of experimental contexts. We found that given the opportunity, tree crickets optimised baffle acoustics; they selected the best sized object and modified it appropriately to make a near optimal baffle. Surprisingly, optimization could be achieved in a single attempt, and is likely to be achieved through an inherited yet highly accurate behavioural heuristic.