The ground offers acoustic efficiency gains for crickets and other calling animals.

Male crickets attract females by producing calls with their forewings. Louder calls travel further and are more effective at attracting mates. However, crickets are much smaller than the wavelength of their call, and this limits their power output. A small group called tree crickets make acoustic tools called baffles which reduce acoustic short-circuiting, a source of dipole inefficiency. Here, we ask why baffling is uncommon among crickets. We hypothesize that baffling may be rare because like other tools they offer insufficient advantage for most species. To test this, we modelled the calling efficiencies of crickets within the full space of possible natural wing sizes and call frequencies, in multiple acoustic environments. We then generated efficiency landscapes, within which we plotted 112 cricket species across 7 phylogenetic clades. We found that all sampled crickets, in all conditions, could gain efficiency from tool use. Surprisingly, we also found that calling from the ground significantly increased efficiency, with or without a baffle, by as much as an order of magnitude. We found that the ground provides some reduction of acoustic short-circuiting but also halves the air volume within which sound is radiated. It simultaneously reflects sound upwards, allowing recapture of a significant amount of acoustic energy through constructive interference. Thus, using the ground as a reflective baffle is an effective strategy for increasing calling efficiency. Indeed, theory suggests that this increase in efficiency is accessible not just to crickets but to all acoustically communicating animals whether they are dipole or monopole sound sources.

Biomechanical origins of proprioceptor feature selectivity and topographic maps in the Drosophila leg.

Our ability to sense and move our bodies relies on proprioceptors, sensory neurons that detect mechanical forces within the body. Different subtypes of proprioceptors detect different kinematic features, such as joint position, movement, and vibration, but the mechanisms that underlie proprioceptor feature selectivity remain poorly understood. Using single-nucleus RNA sequencing (RNA-seq), we found that proprioceptor subtypes in the Drosophila leg lack differential expression of mechanosensitive ion channels. However, anatomical reconstruction of the proprioceptors and connected tendons revealed major biomechanical differences between subtypes. We built a model of the proprioceptors and tendons that identified a biomechanical mechanism for joint angle selectivity and predicted the existence of a topographic map of joint angle, which we confirmed using calcium imaging. Our findings suggest that biomechanical specialization is a key determinant of proprioceptor feature selectivity in Drosophila. More broadly, the discovery of proprioceptive maps reveals common organizational principles between proprioception and other topographically organized sensory systems.

A numerical approach to investigating the mechanisms behind tonotopy in the bush-cricket inner-ear.

Bush-crickets (or katydids) have sophisticated and ultrasonic ears located in the tibia of their forelegs, with a working mechanism analogous to the mammalian auditory system. Their inner-ears are endowed with an easily accessible hearing organ, the crista acustica (CA), possessing a spatial organisation that allows for different frequencies to be processed at specific graded locations within the structure. Similar to the basilar membrane in the mammalian ear, the CA contains mechanosensory receptors which are activated through the frequency dependent displacement of the CA. While this tonotopical arrangement is generally attributed to the gradual stiffness and mass changes along the hearing organ, the mechanisms behind it have not been analysed in detail. In this study, we take a numerical approach to investigate this mechanism in the Copiphora gorgonensis ear. In addition, we propose and test the effect of the different vibration transmission mechanisms on the displacement of the CA. The investigation was carried out by conducting finite-element analysis on a three-dimensional, idealised geometry of the C. gorgonensis inner-ear, which was based on precise measurements. The numerical results suggested that (i) even the mildest assumptions about stiffness and mass gradients allow for tonotopy to emerge, and (ii) the loading area and location for the transmission of the acoustic vibrations play a major role in the formation of tonotopy.

Jump takeoff in a small jumping spider.

Jumping in animals presents an interesting locomotory strategy as it requires the generation of large forces and accurate timing. Jumping in arachnids is further complicated by their semi-hydraulic locomotion system. Among arachnids, jumping spiders (Family Salticidae) are agile and dexterous jumpers. However, less is known about jumping in small salticid species. Here we used Habronattus conjunctus, a small jumping spider (body length ~ 4.5 mm) to examine its jumping performance and compare it to that of other jumping spiders and insects. We also explored how legs are used during the takeoff phase of jumps. Jumps were staged between two raised platforms. We analyzed jumping videos with DeepLabCut to track 21 points on the cephalothorax, abdomen, and legs. By analyzing leg liftoff and extension patterns, we found evidence that H. conjunctus primarily uses the third legs to power jumps. We also found that H. conjunctus jumps achieve lower takeoff speeds and accelerations than most other jumping arthropods, including other jumping spiders. Habronattus conjunctus takeoff time was similar to other jumping arthropods of the same body mass. We discuss the mechanical benefits and drawbacks of a semi-hydraulic system of locomotion and consider how small spiders may extract dexterous jumps from this locomotor system.

Overtone focusing in biphonic tuvan throat singing.

Khoomei is a unique singing style originating from the republic of Tuva in central Asia. Singers produce two pitches simultaneously: a booming low-frequency rumble alongside a hovering high-pitched whistle-like tone. The biomechanics of this biphonation are not well-understood. Here, we use sound analysis, dynamic magnetic resonance imaging, and vocal tract modeling to demonstrate how biphonation is achieved by modulating vocal tract morphology. Tuvan singers show remarkable control in shaping their vocal tract to narrowly focus the harmonics (or overtones) emanating from their vocal cords. The biphonic sound is a combination of the fundamental pitch and a focused filter state, which is at the higher pitch (1-2 kHz) and formed by merging two formants, thereby greatly enhancing sound-production in a very narrow frequency range. Most importantly, we demonstrate that this biphonation is a phenomenon arising from linear filtering rather than from a nonlinear source.

The republic of Tuva, a remote territory in southern Russia located on the border with Mongolia, is perhaps best known for its vast mountainous geography and the unique cultural practice of "throat singing". These singers simultaneously create two different pitches: a low-pitched drone, along with a hovering whistle above it. This practice has deep cultural roots and has now been shared more broadly via world music performances and the 1999 documentary Genghis Blues. Despite many scientists being fascinated by throat singing, it was unclear precisely how throat singers could create two unique pitches. Singing and speaking in general involves making sounds by vibrating the vocal cords found deep in the throat, and then shaping those sounds with the tongue, teeth and lips as they move up the vocal tract and out of the body. Previous studies using static images taken with magnetic resonance imaging (MRI) suggested how Tuvan singers might produce the two pitches, but a mechanistic understanding of throat singing was far from complete. Now, Bergevin et al. have better pinpointed how throat singers can produce their unique sound. The analysis involved high quality audio recordings of three Tuvan singers and dynamic MRI recordings of the movements of one of those singers. The images showed changes in the singer's vocal tract as they sang inside an MRI scanner, providing key information needed to create a computer model of the process. This approach revealed that Tuvan singers can create two pitches simultaneously by forming precise constrictions in their vocal tract. One key constriction occurs when tip of the tongue nearly touches a ridge on the roof of the mouth, and a second constriction is formed by the base of the tongue. The computer model helped explain that these two constrictions produce the distinctive sounds of throat singing by selectively amplifying a narrow set of high frequency notes that are made by the vocal cords. Together these discoveries show how very small, targeted movements of the tongue can produce distinctive sounds.

Evidence supporting synchrony between two active ears due to interaural coupling.

Motivated by recent developments suggesting that interaural coupling in non-mammals allows for the two active ears to effectively synchronize, this report describes otoacoustic measurements made in the oral cavity of lizards. As expected from that model, spontaneous otoacoustic emissions (SOAEs) were readily measurable in the mouth, which is contiguous with the interaural airspace. Additionally, finite element model calculations were made to simulate the interaural acoustics based upon SOAE-related tympanic membrane vibrational data. Taken together, these data support the notion of two active ears synchronizing by virtue of acoustic coupling and have potential implications for sound localization at low-levels.

In that vein: inflated wing veins contribute to butterfly hearing.

Insects have evolved a diversity of hearing organs specialized to detect sounds critical for survival. We report on a unique structure on butterfly wings that enhances hearing. The Satyrini are a diverse group of butterflies occurring throughout the world. One of their distinguishing features is a conspicuous swelling of their forewing vein, but the functional significance of this structure is unknown. Here, we show that wing vein inflations function in hearing. Using the common wood nymph, Cercyonis pegala, as a model, we show that (i) these butterflies have ears on their forewings that are most sensitive to low frequency sounds (less than 5 kHz); (ii) inflated wing veins are directly connected to the ears; and (iii) when vein inflations are ablated, sensitivity to low frequency sounds is impaired. We propose that inflated veins contribute to low frequency hearing by impedance matching.

The Drivers of Heuristic Optimization in Insect Object Manufacture and Use.

Insects have small brains and heuristics or 'rules of thumb' are proposed here to be a good model for how insects optimize the objects they make and use. Generally, heuristics are thought to increase the speed of decision making by reducing the computational resources needed for making decisions. By corollary, heuristic decisions are also deemed to impose a compromise in decision accuracy. Using examples from object optimization behavior in insects, we will argue that heuristics do not inevitably imply a lower computational burden or lower decision accuracy. We also show that heuristic optimization may be driven by certain features of the optimization problem itself: the properties of the object being optimized, the biology of the insect, and the properties of the function being optimized. We also delineate the structural conditions under which heuristic optimization may achieve accuracy equivalent to or better than more fine-grained and onerous optimization methods.

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.

Stay tuned: active amplification tunes tree cricket ears to track temperature-dependent song frequency.

Tree cricket males produce tonal songs, used for mate attraction and male-male interactions. Active mechanics tunes hearing to conspecific song frequency. However, tree cricket song frequency increases with temperature, presenting a problem for tuned listeners. We show that the actively amplified frequency increases with temperature, thus shifting mechanical and neuronal auditory tuning to maintain a match with conspecific song frequency. Active auditory processes are known from several taxa, but their adaptive function has rarely been demonstrated. We show that tree crickets harness active processes to ensure that auditory tuning remains matched to conspecific song frequency, despite changing environmental conditions and signal characteristics. Adaptive tuning allows tree crickets to selectively detect potential mates or rivals over large distances and is likely to bestow a strong selective advantage by reducing mate-finding effort and facilitating intermale interactions.

Active amplification in insect ears: mechanics, models and molecules.

Active amplification in auditory systems is a unique and sophisticated mechanism that expends energy in amplifying the mechanical input to the auditory system, to increase its sensitivity and acuity. Although known for decades from vertebrates, active auditory amplification was only discovered in insects relatively recently. It was first discovered from two dipterans, mosquitoes and flies, who hear with their light and compliant antennae; only recently has it been observed in the stiffer and heavier tympanal ears of an orthopteran. The discovery of active amplification in two distinct insect lineages with independently evolved ears, suggests that the trait may be ancestral, and other insects may possess it as well. This opens up extensive research possibilities in the field of acoustic communication, not just in auditory biophysics, but also in behaviour and neurobiology. The scope of this review is to establish benchmarks for identifying the presence of active amplification in an auditory system and to review the evidence we currently have from different insect ears. I also review some of the models that have been posited to explain the mechanism, both from vertebrates and insects and then review the current mechanical, neurobiological and genetic evidence for each of these models.

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.

A tympanal insect ear exploits a critical oscillator for active amplification and tuning.

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. The tuning of the antennal ears of mosquitoes and flies, however, arises from active amplification, a process similar to that at work in the mammalian cochlea. Yet, the presence of active amplification in the other type of insect ears--tympanal ears--has remained uncertain. 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.

Low-pass filters and differential tympanal tuning in a paleotropical bushcricket with an unusually low frequency call.

Low-frequency sounds are advantageous for long-range acoustic signal transmission, but for small animals they constitute a challenge for signal detection and localization. The efficient detection of sound in insects is enhanced by mechanical resonance either in the tracheal or tympanal system before subsequent neuronal amplification. Making small structures resonant at low sound frequencies poses challenges for insects and has not been adequately studied. Similarly, detecting the direction of long-wavelength sound using interaural signal amplitude and/or phase differences is difficult for small animals. Pseudophylline bushcrickets predominantly call at high, often ultrasonic frequencies, but a few paleotropical species use lower frequencies. We investigated the mechanical frequency tuning of the tympana of one such species, Onomarchus uninotatus, a large bushcricket that produces a narrow bandwidth call at an unusually low carrier frequency of 3.2 kHz. Onomarchus uninotatus, like most bushcrickets, has two large tympanal membranes on each fore-tibia. We found that both these membranes vibrate like hinged flaps anchored at the dorsal wall and do not show higher modes of vibration in the frequency range investigated (1.5-20 kHz). The anterior tympanal membrane acts as a low-pass filter, attenuating sounds at frequencies above 3.5 kHz, in contrast to the high-pass filter characteristic of other bushcricket tympana. Responses to higher frequencies are partitioned to the posterior tympanal membrane, which shows maximal sensitivity at several broad frequency ranges, peaking at 3.1, 7.4 and 14.4 kHz. This partitioning between the two tympanal membranes constitutes an unusual feature of peripheral auditory processing in insects. The complex tracheal shape of O. uninotatus also deviates from the known tube or horn shapes associated with simple band-pass or high-pass amplification of tracheal input to the tympana. Interestingly, while the anterior tympanal membrane shows directional sensitivity at conspecific call frequencies, the posterior tympanal membrane is not directional at conspecific frequencies and instead shows directionality at higher frequencies.

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.

Animals communicate in non-ideal and noisy conditions. The primary method they use to improve communication efficiency is sender-receiver matching: the receiver's 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.

Predicting acoustic orientation in complex real-world environments.

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.

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

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.

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

The sequencing of the Mycobacterium 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 approximately 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.