Figure 1 - uploaded by Charlie Woodrow
Content may be subject to copyright.
![Morphology of the foretibial organ of Cyphoderris monstrosa and phylogenetic context. (a) Location of the foretibial organ and anatomy of the prothoracic trachea, which is not specialized for sound conduction in this species. (b) External anatomy of the foretibial organ, with the two key parts of the tympanum highlighted. (c) Cross-sectional anatomy of the foretibial organ of C. monstrosa. (d ) Phylogeny of tympanal ears in the Ensifera mentioned in this study, with an example of a Jurassic prophalangopsid (Hagloidea) indicated with arrow. Labels: ca, crista acustica; dw, dorsal wall; atm, anterior tympanal membrane; ptm, posterior tympanal membrane; s, septum; hc, haemolymph channel (liquid filled); at, acoustic tracheae (air-filled). d modified from Song et al. [33]. Fossil prophalangopsid in d from Gu et al. [31]. (Online version in colour.)](publication/360224897/figure/fig1/AS:1151564039356416@1651565670445/Morphology-of-the-foretibial-organ-of-Cyphoderris-monstrosa-and-phylogenetic-context-a.png)
Morphology of the foretibial organ of Cyphoderris monstrosa and phylogenetic context. (a) Location of the foretibial organ and anatomy of the prothoracic trachea, which is not specialized for sound conduction in this species. (b) External anatomy of the foretibial organ, with the two key parts of the tympanum highlighted. (c) Cross-sectional anatomy of the foretibial organ of C. monstrosa. (d ) Phylogeny of tympanal ears in the Ensifera mentioned in this study, with an example of a Jurassic prophalangopsid (Hagloidea) indicated with arrow. Labels: ca, crista acustica; dw, dorsal wall; atm, anterior tympanal membrane; ptm, posterior tympanal membrane; s, septum; hc, haemolymph channel (liquid filled); at, acoustic tracheae (air-filled). d modified from Song et al. [33]. Fossil prophalangopsid in d from Gu et al. [31]. (Online version in colour.)
Source publication
Ensiferan orthopterans offer a key study system for acoustic communication and the process of insect hearing. Cyphoderris monstrosa (Hagloidea) belongs to a relict ensiferan family and is often used for evolutionary comparisons between bushcrickets (Tettigoniidae) and their ancestors. Understanding how this species processes sound is therefore vita...
Contexts in source publication
Context 1
... the tettigoniids, C. monstrosa possesses two paired tympana (anterior and posterior, or ATM and PTM, respectively) on each foreleg, backed by air-filled trachea, at the proximal ends of the foretibiae ( figure 1a,b). The tympana have a thick region, and a thinner membranous region along the ventral edge. ...
Context 2
... reception in C. monstrosa is not specialized through this trachea but only externally on the tympanum surface [26]. Internally, the ear consists of two enlarged branches of the tracheal system with the auditory chordotonal organ, the CA, lying dorsally above the anterior tracheal branch ( figure 1c). In C. monstrosa, these branches are symmetrical. ...
Context 3
... the Tettigoniidae, there is an asymmetry that favours the anterior branch, which displays a flat and unilaterally widening dorsal surface, referred to as the dorsal wall (DW). Such a morphological specialization of the DW is not present in C. monstrosa ( figure 1c). Externally, the foretibial organ resembles those of the Jurassic Prophalangopsidae more than those of extant relatives ( figure 1d). ...
Context 4
... a morphological specialization of the DW is not present in C. monstrosa ( figure 1c). Externally, the foretibial organ resembles those of the Jurassic Prophalangopsidae more than those of extant relatives ( figure 1d). ...
Context 5
... well as stimulating the system with broadband stimuli, four-cycle pure tone stimuli were presented to the ear and recorded in the time domain to ensure the tonotopy was not an artefact of the broadband stimulation. Owing to the previous works on this species [26,28], the frequencies chosen for pure tone stimulation were 12.5 kHz (the average peak calling song frequency of the species under our rearing conditions; electronic supplementary material, figure S1) and 2 kHz (which has been previously found to be the best tuning of the auditory sensory neurons). Pure tone responses confirmed the observation seen in the broadband stimulation experiments (figure 2), whereby the maximum region of displacement of the tympanum differed depending on the frequency of stimulation, with the 2 kHz tone displaying maximum velocity of 151.9 ± 105.6 nm s −1 Pa in the proximal end of the tympanum, and the 12.5 kHz tone displaying a maximum velocity of 508.1 ± 339.7 nm s −1 Pa in the distal region ( figure 3a). ...
Context 6
... the foretibial organ of C. monstrosa, the tracheal branches are symmetrical, and ovular in cross section (figure 1). The CA lies above the anterior tracheal branch, as with modern tettigoniids ( figure 1; [14]). The ear of C. monstrosa must therefore exploit tonotopic resonances of the tympanum to localize vibrations to different points along the anterior tracheal branch, which in turn activates the nearest mechanoreceptors, which are not directly connected to the tympana. ...
Context 7
... auditory thresholds around the calling song frequency may not be such a problem for conspecific communication in this species, as the male calling song is extremely loud (over 100 dB re. 20 µPa at 20 cm; electronic supplementary material, figure S1). The spatial disparity between the CA and the distal tympanal displacement within the ear could be reduced over time if high ear sensitivity was selected for, because reducing the distance between the mechanoreceptors and peripheral displacement would result in reduced attenuation of the signal throughout the ear for greater mechanical displacement of the chordotonal organ. ...
Citations
... The field cricket anterior tracheal branch (ATB) is distinct compared to other more arboreal ensiferans: Eneopeterinae [21], Oecanthinae [24], Tettigoniidae [25] and Hagloidea [26]. Unlike these taxa, the Gryllinae ATB is not in direct contact with the ATM and is considerably smaller than the PTB (see figure 2c). ...
Many animals employ a second frequency filter beyond the initial filtering of the eardrum (or tympanal membrane). In the field cricket ear, both the filtering mechanism and the transmission path from the posterior tympanal membrane (PTM) have remained unclear. A mismatch between PTM vibrations and sensilla tuning has prompted speculations of a second filter. PTM coupling to the tracheal branches is suggested to support a transmission pathway. Here, we present three independent lines of evidence converging on the same conclusion: the existence of a series of linked membranes with distinct resonant frequencies serving both filtering and transmission functions. Micro-computed tomography (µ-CT) highlighted the ‘dividing membrane (DivM)’, separating the tracheal branches and connected to the PTM via the dorsal membrane of the posterior tracheal branch (DM-PTB). Thickness analysis showed the DivM to share significant thinness similarity with the PTM. Laser Doppler vibrometry indicated the first of two PTM vibrational peaks, at 6 and 14 kHz, originates not from the PTM but from the coupled DM-PTB. This result was corroborated by µ-CT-based finite element analysis. These findings clarify further the biophysical source of neuroethological pathways in what is an important model of behavioural neuroscience. Tuned microscale coupled membranes may also hold biomimetic relevance.
... 30 The emergence of pinnae coincides with the formation of a tonotopic fluid-filled inner ear (auditory vesicle) for enhanced frequency analysis across a large dynamic range. 31 The outer ear structures are fundamental for establishing the overall auditory range of the katydid and function together to make the ear a uniquely wide-spectrum sound receiver. However, the evolutionary history of this hearing system is still not well understood, and no studies have been able to connect sound production and sound reception in katydids through deep time because of a lack of materials and methodologies. ...
... 41 Instead, they process frequency at the most peripheral level through tonotopy of the tympanum, transmitting the vibrations laterally from tympanum to primitive CA via the DW. 31 E. handlirschi is a small katydid of the subfamily Lipotactinae. 36,42 The holotype presented here is a male and measures just 8.98 mm from head to tip of the abdomen. ...
... 27 This differs from their sister clades, as evidenced by living Prophalangopsidae with leg tracheae lacking an acoustic function. 31 In such pressure-difference receiver, the mechanical displacement of the tympanum is dictated by the inputs to both sides of the ear 54,55 and is usually aided by reduced velocity of sound propagating within the EC. 56 This velocity will depend on the radius of ...
Article An Eocene insect could hear conspecific ultrasounds and bat echolocation Graphical abstract Highlights d A 44-million-year-old amber fossil katydid reveals exquisite ear preservation d Biophysics of wings reveals this species utilized ultrasounds for communication d Modeling of auditory range demonstrates tuning to male sexual signal, as well as to bat cries d Ultrasound discrimination in insects was established by the Eocene Authors Charlie Woodrow, Emine Celiker, Fernando Montealegre-Z Correspondence charlie.woodrow@ebc.uu.se (C.W.), fmontealegrez@lincoln.ac.uk (F.M.-Z.) In brief Woodrow et al. show auditory tuning to male acoustic signals and extended ultrasonic hearing for predator detection in the ear of an Eocene katydid. This remarkable fossil pushes back the evolution of complex auditory processing in insects and suggests that acoustic communication strategies in katydids diversified during the emergence of echolocating bats. SUMMARY Hearing has evolved independently many times in the animal kingdom and is prominent in various insects and vertebrates for conspecific communication and predator detection. Among insects, katydid (Orthoptera: Tet-tigoniidae) ears are unique, as they have evolved outer, middle, and inner ear components, analogous in their biophysical principles to the mammalian ear. The katydid ear consists of two paired tympana located in each foreleg. These tympana receive sound externally on the tympanum surface (usually via pinnae) or internally via an ear canal (EC). The EC functions to capture conspecific calls and low frequencies, while the pinnae passively amplify higher-frequency ultrasounds including bat echolocation. Together, these outer ear components provide enhanced hearing sensitivity across a dynamic range of over 100 kHz. However, despite a growing understanding of the biophysics and function of the katydid ear, its precise emergence and evolutionary history remains elusive. Here, using microcomputed tomography (mCT) scanning, we recovered ge-ometries of the outer ear components and wings of an exceptionally well-preserved katydid fossilized in Baltic amber ($44 million years [Ma]). Using numerical and theoretical modeling of the wings, we show that this species was communicating at a peak frequency of 31.62 (± 2.27) kHz, and we demonstrate that the ear was biophysically tuned to this signal and to providing hearing at higher-frequency ultrasounds (>80 kHz), likely for enhanced predator detection. The results indicate that the evolution of the unique ear of the katydid, with its broadband ultrasonic sensitivity and analogous biophysical properties to the ears of mammals, emerged in the Eocene.
... Future work, currently in progress with the data from this project, aims to connect form to function; using numerical models to demonstrate how changes to the size and shape of the ear canal relate to differences in auditory tuning. While the final findings of this project are still being analyzed for publication, some of the data has already been utilized in studies of ear evolution, auditory biophysics, and to supplement taxonomic contributions (Woodrow et al. 2022;Woodrow and Montealegre-Z 2023;Celiker et al. 2022;Hemp et al. 2023), highlighting the need for such comparative studies. I hope to soon make the full datasets from this project available in an open access form for shared use and I am excited to see how it will be used in the future. ...
This report is a summary of a Theodore J. Cohn grant to investigate the diversity of the katydid ear canal awarded as part of the PhD of CW. The full results of this report are in preparation for future peer-reviewed dissemination.
... evolution of acoustic organs and behavior (1,(8)(9)(10). Male katydids produce sounds through friction between specialized veins of the forewings (tegminal stridulation), and these sounds are received by males and females primarily through the ears (auditory tympana) on the protibiae (11) (Fig. 1A). ...
... Our fossils represent the earliest-known insect ears and extend the age range of the modern-type auditory tympana by 100 million years to the Middle Jurassic. In general morphology and size, the fossil ears are identical to those observed in modern Prophalangopsidae and some Stenopelmatidae, representing an ancestral character of the ear (9,11,24). Correspondingly, these extinct prophalangopsids probably had evolved similar biomechanics to extant "ancestral" forms of ensiferans like Anoatostomatidae and Prophalangopsidae, the class 2 lever model (38). In this model, the stiff tympanal plate acts as a hinge with the dorsal edge connected to the cuticle of the leg and forms the fulcrum of a lever that can move a load between the fulcrum and the force, effectively transmitting mechanical energy to the fluid environment of the sensory organ (38,39). ...
... Some Daohugou katydids produced a comparatively low-frequency song, which is a long-distance advertising signal (43). Such a long-distance communication system requires the evolution of directional sensitivity (44,45), suggesting that the conspecific females likely had evolved directional hearing, similar to extant Prophalangopsidae (9,46). In addition, female katydids cannot produce sounds and the ears of male katydids are used for intermale acoustic communication, which is an important way for intermale territorial and aggressive behaviors to be resolved in orthopterans (11,40). ...
Acoustic communication has played a key role in the evolution of a wide variety of vertebrates and insects. However, the reconstruction of ancient acoustic signals is challenging due to the extreme rarity of fossilized organs. Here, we report the earliest tympanal ears and sound-producing system (stridulatory apparatus) found in exceptionally preserved Mesozoic katydids. We present a database of the stridulatory apparatus and wing morphology of Mesozoic katydids and further calculate their probable singing frequencies and analyze the evolution of their acoustic communication. Our suite of analyses demonstrates that katydids evolved complex acoustic communication including mating signals, intermale communication, and directional hearing, at least by the Middle Jurassic. Additionally, katydids evolved a high diversity of singing frequencies including high-frequency musical calls, accompanied by acoustic niche partitioning at least by the Late Triassic, suggesting that acoustic communication might have been an important driver in the early radiation of these insects. The Early-Middle Jurassic katydid transition from Haglidae- to Prophalangopsidae-dominated faunas coincided with the diversification of derived mammalian clades and improvement of hearing in early mammals, supporting the hypothesis of the acoustic coevolution of mammals and katydids. Our findings not only highlight the ecological significance of insects in the Mesozoic soundscape but also contribute to our understanding of how acoustic communication has influenced animal evolution.
... Analogous travelling waves have also been measured invasively and non-invasively in the ears of bushcrickets (3,4,14,15). The underlying mechanism is likely more ancient since it has been observed in grigs, suggesting it was shared by a common ancestor (16). ...
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.
