Review Article Journal of Orthoptera Research 2019, 28(2): 205-219 What determines the number of auditory sensilla in the tympanal hearing organs of Tettigoniidae? Perspectives from comparative neuroanatomy and evolutionary forces JOHANNES STRAUB! 1 AG Integrative Sensory Physiology, Institute for Animal Physiology, Justus-Liebig-Universitat GiefSen, Germany. Corresponding author: Johannes Strauf? (johannes.strauss@ physzool.bio.uni-giessen.de) Academic editor: Diptarup Nandi | Received 1 February 2019 | Accepted 15 May 2019 | Published 2 October 2019 http://zoobank.org/BEBC7E8A-D058-4E65-A6CA-079 CAD8E6B17 Citation: Strauf J (2019) What determines the number of auditory sensilla in the tympanal hearing organs of Tettigoniidae? Perspectives from comparative neuroanatomy and evolutionary forces. Journal of Orthoptera Research 28(2): 205-219. https://doi.org/10.3897/jor.28.33586 Abstract Insects have evolved complex receptor organs for the major sensory modalities. For the sense of hearing, the tympanal organ of Tettigoniidae (bush crickets or katydids) shows remarkable convergence to vertebrate hearing by impedance conversion and tonotopic frequency analysis. The main auditory receptors are scolopidial sensilla in the crista acustica. Mor- phological studies established that the numbers of auditory sensilla are species-specific. However, the factors determining the specific number of auditory sensilla are not well understood. This review provides an over- view of the functional organization of the auditory organ in Tettigoniidae, including the diversification of the crista acustica sensilla, a list of species with the numbers of auditory sensilla, and a discussion of evolutionary forces affecting the number of sensilla in the crista acustica and their sensi- tivity. While all species of Tettigoniidae studied so far have a crista acustica, the number of sensilla varies on average from 15-116. While the relative differences or divergence in sensillum numbers may be explained by adap- tive or regressive changes, it is more difficult to explain a specific number of sensilla in the crista acustica of a specific species (like for the model species Ancistrura nigrovittata, Copiphora gorgonensis, Gampsocleis gratiosa, Mecopoda elongata, Requena verticalis, or Tettigonia viridissima): sexual and natural selection as well as allometric relationships have been identified as key factors influencing the number of sensilla. Sexual selection affects the number of auditory sensilla in the crista acustica by the communication system and call patterns. Further, positive allometric relationships indicate positive selection for certain traits. Loss of selection leads to evolutionary regression of the auditory system and reduced number of auditory sensilla. This diversity in the auditory sensilla can be best addressed by comparative studies reconstructing adaptive or regressive changes in the crista acustica. Keywords acoustic communication, behavior, crista acustica, katydid, sexual selection Acoustic communication and behavior of Tettigoniidae The study of insect hearing is an interdisciplinary field of re- search that has highlighted the great diversity of tympanal organs in different taxa (Fullard and Yack 1993, Hoy and Robert 1996, Yager 1999, Stumpner and von Helversen 2001, Yack 2004, Yack and Dawson 2007, R6mer 2018). The tympanal organs in insects usually consist of one or two tympanal membranes, a tracheal sack, and a scolopidial organ containing sensory neurons (Hoy 1998, Yager 1999, Yack 2004, ROmer 2018). Tympanal hearing organs occur on almost all locations of the insect body and with a great variation in the number of sensory neurons (scolopidial sensilla) associated with the tympanal membranes. The sensilla numbers can vary between only one in notodontid moth and hawkmoth up to 2000 in cicadas and (atympanate) bladder grass- hoppers (Yager 1999, Yack 2004, Straufg$ and Stumpner 2015). For several tympanal ears, sensillum numbers range between 20-100 auditory sensilla (Yager 1999), and within Orthoptera, locusts and crickets usually have 50-70 auditory sensilla. Differences in the set of sensilla have been discussed for adaptive modifications relat- ing to specific hearing functions (e.g., Strauf$ and Stumpner 2015). In Tettigoniidae, the tympanal organs are located in the proximal tibia of the forelegs, with tympanal membranes at the anterior and posterior side (Fig. 1A). These hearing organs with auditory sensil- la in the crista acustica (CA) are generally broadly tuned and cover frequency ranges from low sound into ultrasonic frequencies (e.g., Kalmring et al. 1990, Rossler and Kalmring 1994, Rossler et al. 1994, Schul and Patterson 2003). With more than 6500 species (Ingrisch and Rentz 2009, Mu- gleston et al. 2013), Tettigoniidae are an ideal taxon to study prox- imate and ultimate aspects of acoustic signalling and the design and diversification of ears. Hearing in Ensifera in general and in tettigoniids in particular likely evolved for detection and localiza- tion of potential mates (Bailey 1991, Stumpner and von Helversen 2001, Robinson and Hall 2002, Greenfield 2016) by calls that are species-specific in temporal pattern (Gwynne 2001, Robinson and Hall 2002). Male tettigoniids usually produce acoustic signals by tegminal stridulation, and females perform phonotaxis towards the males (unidirectional communication system). However, this signalling system was expanded into duets with females produc- ing a reply call in few tettigoniid taxa (bidirectional communica- tion system) (Nickle and Carlysle 1975, Bailey 2003, Heller et al. 2015), and males or both sexes move towards the other signaller. Selection requires the sensitivity for conspecific call frequencies and the recognition of the temporal pattern in the conspecific sig- nals over other species’ signals. While highest auditory sensitivity JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 206 can match with the carrier frequency of the calls, there are also cases of mismatches between their call spectra and the frequency tuning of the ears known (e.g., Bailey and R6mer 1991, ROmer and Bailey 1998, see also Mason 1991 for a mismatch in the pro- phalangopsid Cyphoderris monstrosa). The transmission of sound signals is highly influenced by the environment, as vegetation fil- ters particularly higher frequency components depending on the distance (ROmer and Lewald 1992, Robinson and Hall 2002). Hearing further allows predator detection and evasion, male aggressive behavior, and male spacing (Bailey 1985, 1991, Gwyn- ne 2001, Robinson and Hall 2002). In particular, echolocating bats are important predators of tettigoniids (Belwood 1990, Kalka et al. 2008, Jones et al. 2014, ter Hofstede et al. 2017). Since bats evolved after the appearance of stridulatory structures in Tettigoni- idae, the evolutionary sequence of hearing is likely to first involve intraspecific communication and then have expanded to higher ultrasonic ranges to include bat detection (Bailey 1991, Hoy 1992, Stumpner and von Helversen 2001, Greenfield 2016), while early insectivorous mammals likely also preyed upon stridulating in- sect (Hoy 1992). Tettigoniidae can hear bat echolocation calls and developed behavioral responses (Pollack 2015): certain spe- cies stop calling as it exposes the signaller (Faure and Hoy 2000, ter Hofstede et al. 2010), or animals in flight evade the sound source by dropping (Libersat and Hoy 1991) or changing flight orientation (Schulze and Schul 2001, Kilmer et al. 2010). In the tonotopically ordered CA (see below), the frequency contents of intraspecific calls or bat echolocation calls are processed by the adequately tuned sensilla. This tonotopic organization also allows intensity (distance) analysis (Hennig et al. 2004, Stumpner and Nowotny 2014, Romer 2016): further populations of sensilla will get recruited if the stimulus amplitudes increase to levels that also excite sensory neurons tuned to different best frequencies (H6bel and Schul 2007). The recruitment of sensilla for intensity discrimi- nation is well documented for Requena verticalis with 22 auditory sensilla (ROmer et al. 1998, Romer 2016). With the species-specific number of auditory sensilla and length of the auditory organ, the differences in thresholds extend the dynamic range of the hearing organ, and the number of sensilla can not only influence the ac- curacy of representing frequency resolution but also of amplitude differences (R6mer 2016). Selection and evolutionary adaptations of the tettigoniid hearing organ Selection acts in a complex setting of acoustic signalling that in- cludes the communication system, signal transmission, signalling distance (active space), and background noise. By the functions of hearing in mate detection and predator evasion, both sexual and natural selection affect the hearing organs in Tettigoniidae. Adap- tations are notable in particular in the size differences of spiracles, which can be related to specific acoustic behaviors and selection pressures between sexes (e.g., Bailey and Romer 1991, Heller et al. 1997a, Mason and Bailey 1998, Strauf et al. 2017). In some circumstances, evolutionary forces may be difficult to identify by studying only the phenotypes, as selection pressures may overlap or even act in different directions (see Straufg and Stumpner 2015). After the loss of sexual selection, especially regressive evolution— in general, the decrease or reduction of a specific structure in some dimension like size, length, or number of elements—has been noted for spiracles and tympana, and this can also be analyzed for effects on the CA (the reduction of sensillum numbers) in a com- parative approach. Drawing on the literature for several tettigoniid J. STRAUS groups, here the neuroanatomical and physiological evidence for adaptations in the number of auditory sensilla in the CA is sum- marized and discussed. Anatomical and neuronal structures of the tettigoniid tym- panal hearing organ The auditory organ in tettigoniids follows a ground plan of neuronal and anatomical elements, which can vary considerably in their morphology across different species (Bailey 1990, 1993, Lakes and Schikorski 1990, Rodssler et al. 2006). These hearing organs show a remarkable evolutionary convergence to the ver- tebrate hearing organs for impedance conversion and frequency representation (Montealegre-Z et al. 2012, Palghat Udayashankar et al. 2012, Hildebrandt 2014). The tympanal membranes are areas of thinned cuticle. The membranes can be openly exposed, but in other species can also be located behind tympanal covers or tympanal flaps (Bailey 1993). In the latter cases, sound enters to the tympana through thin tympanal slits (Fig. 1B, C). These flaps are supposed to con- tribute to the directionality of hearing (Bailey and Stephen 1978, Mason et al. 1991, Bailey 1993). In some species, so-called pin- nae form around the tympana which leave a broader slit over the tympana (Bailey 1993). In some species like the Australian Bei- ericolya tardipes (Meconematinae), the Peruvian Bufotettix auche- nacophoroides (Pseudophyllinae), and the Asian Lacipoda immunda (Pseudophyllinae), the proximal tibia is swollen so that it forms cups around the tympana and orients the opening dorsally on the tibia (Bailey 1990, Rentz 2001, Nickle 2006). The cup formation is described as most elaborated in Phisis and Decolya (Meconema- tinae) (Bailey 1990). The neuronal responses to sound entering via the tympanal membranes are stronger for relatively lower frequencies (Hum- mel et al. 2011, Stumpner and Nowotny 2014), and low frequency sound travels relatively poor in the acoustic trachea (Jonsson et al. 2016). Rather than sound acting on the outer surface of the tym- panal membranes, the major input to the hearing organ is via the acoustic spiracle in the prothorax, especially for higher sound fre- quencies (Lewis 1974, Nocke 1975, Michelsen et al. 1994, Bailey 1998, Hummel et al. 2011, Stumpner and Nowotny 2014, Jonsson et al. 2016). This enlarged acoustic spiracle is usually permanently open (for one exception see ROmer and Bailey 1998), and con- tinues into the acoustic bulla in the prothorax and the acoustic trachea that runs through the thorax into the foreleg and passively amplifies the sound input (Bailey 1993, Heinrich et al. 1993). The sizes of the spiracle and bulla differ between species (Mason et al. 1991, Stumpner and Heller 1992, Bailey 1993, Heinrich et al. 1993) and even between sexes of the same species (Bailey and Romer 1991, Heller et al. 1997a, Mason and Bailey 1998, Strauf et al. 2014). In addition, extensive differences in the sizes of bulla and spiracles occur between larger taxonomic groups, e.g., Phaner- opterinae, Pseudophyllinae, and Tettigoniinae (Bailey 1990, 1993, Mason etal. 1991). In the proximal tibia, the acoustic trachea splits into an anterior and posterior branch at the level of the tympana (Fig. 1B; Schwabe 1906, Schumacher 1975a, Lin et al. 1994, Sick- mann et al. 1997), forming a “bicompartmental receptor region” (Heinrich et al. 1993). The split into the two tracheal branches oc- curs only distally of the proximal sensilla of the CA (Rossler et al. 1994, Sickmann et al. 1997). The tracheal branches align laterally behind the anterior and posterior tympanum (Fig. 1B). The principal sensory organ processing acoustic stimuli is the crista acustica (CA) located within the foreleg tibia between the JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUR 207 b distal anterior dorsal dow ——— ne | posterior anterior Fig. 1. The auditory system of bushcrickets. A. Schematic of the acoustic trachea (at) from the acoustic spiracle (as) in the thorax into the foreleg with tympanal membranes (ty) in the proximal tibia; B. Transverse section of the tibia at the level of the tympana and crista acustica in Gampsocleis gratiosa; in Gampsocleis gratiosa; C. The sensory organs in the proximal tibia of the male Tettigonia viridissima. The dorsal cuticle has been removed after axonal tracing of the tympanal nerve with cobalt solution to stain sensory neurons of the subgenual organ (SGO), intermediate organ (IO) and crista acustica. The crista acustica is placed between the anterior tympanum (aty) and posterior tympa- num (pty). The tympanal flaps (tf) cover the tympanal membranes. Arrows indicate the tectorial membrane; D. Morphological differences of sensory neurons along the crista acustica from G. gratiosa, showing the (d,) third-most proximal, (d,.) middle, and (d.,.) third-most distal sensillum. Abbreviations: at, anterior trachea; aty, anterior tympanum; cc, cap cell; de, dendrite; dow, dorsal tracheal wall; hc, haemolymph channel; IO, intermediate organ; nmc, nerve muscle channel; nsc, nucleus of scolopale cell; pn, perikarya of sensory neurons; pt, posterior trachea; pty, posterior tympanum; s, septum; sb, supporting band; scol, scolopale cap and rods; SGO, subgenual organ; sli, slit; sn, sensory neuron; tf, tympanal flap; tm, tectorial membrane. Scales: 500 am (B), 100 pm (C), 50 pm (D). Figure A. reprinted from Strauf et al. 2014, with permission from John Wiley and Sons. B., D. redrawn from Lin et al. 1994, with permission from John Wiley and Sons. JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 208 tympana (Fig. 1C). The sensory neurons are scolopidial sensilla located over the tracheal branches arranged in the proximo-distal axis of the tibia (Fig. 1B-D), covered by the tectorial membrane, which is triangular in shape with a curvilinear surface. The CA is part of the complex tibial organ together with other scolopidial organs: the subgenual organ, the intermediate organ and the ac- cessory organ (Fig. 1C; Lakes and Schikorski 1990, Rossler et al. 2006, Strauf§ et al. 2016). The CA sensilla are attached to the tec- torial membrane and the dorsal wall of the acoustic trachea but are not in direct contact with the tympana (Fig. 1B, D; Lakes and Schikorski 1990). The sensilla are placed dorsally of the acoustic trachea (the dorsal wall) and are mainly arranged linearly. Their dendrites run over the anterior tracheal branch from the anterior to the posterior tibia (Fig. 1B, C) and terminate in cap cells linked to the tectorial membrane (Fig. 1D). The sensilla are overall mor- phologically similar throughout the CA (Lin et al. 1994, Kalmring et al. 1995b) but decrease from proximal to distal in the size of cap cells, along with the width of the tectorial membrane and the width of the dorsal tracheal wall (Fig. 1D) (Rdssler 1992a, Lin et al. 1994, Réssler and Kalmring 1994, Kalmring et al. 1995a, Sickmann et al. 1997, Hummel et al. 2017). This correlates to the physiological changes in sensory tuning of individual sensilla, with their best frequency increasing from lower to higher frequen- cies from the proximal to the distal end of the CA (Zhantiev and Korsunovskaya 1978, Oldfield 1982, Stdlting and Stumpner 1998, Hummel et al. 2017), and forms a tonotopically arranged filter bank that allows frequency analysis (Stdlting and Stumpner 1998, Hennig et al. 2004, Stumpner and Nowotny 2014, Montealegre-Z and Robert 2015). Anatomical variation between species is also expressed in the number of auditory sensilla in the CA. Scolopidial sensilla are primary sensory neurons that send their axon into the corresponding segmental ganglion of the cen- tral nervous system to form synapses with first order interneurons. The tonotopic representation is maintained in the central projec- tion of auditory afferents (ROmer 1983, Stumpner 1996, Stdlting and Stumpner 1998, Baden and Hedwig 2010). For the tonotopi- cal organization, different physiological adaptations have been proposed (Hennig et al. 2004). Morphological changes in the organ size, organ height, dendrite length, and cap cell size cor- relate with the shift in frequency tuning (Hummel et al. 2017, Scherberich et al. 2017). The tonotopic frequency representation is formed by sound-induced travelling waves at the attachment/ cap cells and in certain species also at the acoustic vesicle, a modi- fied part of the haemolymph channel in the dorsal tibia (Mon- tealegre-Z et al. 2012, Palghat Udayashankar et al. 2012, Stumpner and Nowotny 2014, Montealegre-Z and Robert 2015, Sarria-S et al. 2017). In such cases, the integrity of the acoustic vesicles and the lipidic fluid it contains are necessary for expressing travelling waves (Montealegre-Z et al. 2012). The CA also occurs in the atympanate mid- and hind-legs with a gradual decrease in the number of sensilla (Friedrich 1927, 1928, Knetsch 1939, Schumacher 1975b, 1979), but lacks the auditory specializations such as tympanal membranes, an enlarged trachea and tectorial membrane, elaborate supporting bands, or smaller size of scolopale caps (e.g., Lin et al. 1994). The physiology of these atympanate organs remains unresolved (Rossler et al. 2006), but they lack the high sensitivity to airborne sound found in the fore- legs (Réssler 1992b, Kalmring et al. 1994). Notably, some atympa- nate taxa of Ensifera have a sensory organ present in all leg pairs, the crista acustica homologue, that is homologous to the tettigoniid auditory sensilla, with a number of sensilla similar to the forelegs of tympanate bush crickets (Straufg and Lakes-Harlan 2008, 2010). J. STRAUS Physiological responses to airborne sound were noted also from the the subgenual organ (SGO) and the intermediate organ (IO), usually responding to relatively low frequency at high stimu- lus intensities (Kalmring et al. 1994, Stumpner 1996, Hdbel and Schul 2007), though higher frequency responses were found in the distal IO (Stdlting and Stumpner 1998). Both organs also respond with high sensitivity to substrate vibrations (Kalmring et al. 1994). Here, the focus is on the CA as the sensory organ mainly adapted to airborne sound detection. Comparative neuroanatomy of the crista acustica The CA has been investigated in several species of Tettigoni- idae, and these comparative neuroanatomical studies showed that the number of auditory sensilla is species-specific (Knetsch 1939, Schumacher 1979, Lakes and Schikorski 1990). The sensil- lum numbers in closely related species are usually similar but not identical (Lakes and Schikorski 1990). Sensillum numbers for tet- tigoniid species are presented in Table 1, with numbers between a minimum of 12-14 sensilla (Supersonus and Phlugis spp., Me- conematinae; EF Montealegre-Z, personal communication) and a maximum of 116 sensilla (male Ancylecha fenestrata, Phanerop- terinae; Scherberich et al. 2017). In most species, the CA contains 25-35 sensilla. It could be assumed that well-developed hearing organs also tend to increase the number of sensory neurons if pos- sible, e.g., for better signal detection against noise (Stumpner and Nowotny 2014). The number of auditory sensilla is thus an im- portant indicator of the elaboration or regression of the hearing organ when compared within a specific taxon. Within Orthoptera, a higher number of auditory sensilla is found in both crickets and locusts in comparison to Tettigoniidae (crickets: Eibl 1978, Klose 1996; locusts: Michel and Petersen 1982). Within a genus, tettigoniid species usually have highly similar sensillum numbers, though larger differences occasionally occur (Poecilimon; Strauf et al. 2014). The variation in sensillum numbers between individuals from one species is usually very low (Lakes and Schikorski 1990, Réssler 1992b). Slight differences between individuals caused different averages as reported, for example, in T. viridissima (Schumacher 1973, Kalmring et al. 1995a, b, Strauf et al. 2012). Such ranges of differences have been reported for few species, e.g., in Ancistrura nigrovittata the mean number is 37, with rare extremes of 32, 33, and 40 CA sensilla found (Ostrowski and Stumpner 2010). Commonly, the sexes show no differences in the number of CA sensilla. A notable case of dimorphism exists in An- cylecha fenestrata where males have a significantly higher number of auditory sensilla and a longer CA than females (Scherberich et al. 2016, 2017; see below). In another case, males of Ancistrura nigrovittata have on average two sensilla more in the CA than fe- males (Ostrowski and Stumpner 2010). Notably, the number of auditory sensilla is not directly related to the CA length (Schumacher 1979, Lakes and Schikorski 1990, Strauf§ et al. 2017), and between species, fewer sensilla can be found in a longer CA (e.g., Rossler et al. 1994). The scolopidial sensilla can occur highly concentrated in the distal CA (Réssler et al. 1994, Kalmring et al. 1995a), leading to pairs or even triplets of somata at the same proximo-distal level (Sickmann et al. 1997, Strauf$ et al. 2012, Hummel et al. 2017). These findings raise the question of how differences in the number of auditory sensilla relate to the tonotopic frequency analysis, and what factors affect these changes in numbers. For Tettigoniidae, a relatively high number of species have been investigated for the neuroanatomy of the hearing organs. JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS 209 Table 1. Number of auditory sensilla in the crista acustica of Tettigoniidae. If one species is covered by several references, usually the number which includes mean and standard deviation is cited. Relatively large differences in sensillum numbers reported between stud- ies based on different techniques or sample sizes are also referenced for a few species. Species Bradyporinae Deracantha onos Zichya baranovi Conocephalinae: Conocephalini Conocephalus fuscus Conocephalus dorsalis Conocephalus nigropleurum Conocephalinae: Copiphorini Copiphora gorgonensis Neoconocephalus robustus Neoconocephalus bivocatus Neoconocephalus exiliscanorus Neoconocephalus nebrascensis Neoconocephalus ensiger Neoconocephalus triops Neoconocephalus retusus Neoconocephalus palustris Neoconocephalus affinis Mygalopsis marki Ruspolia nitidula (syn. Homorocoryphus nitidulus) Ephippigerinae Ephippiger ephippiger Ephippiger perforatus Uromenus rugosicollis Hetrodinae Acanthoplus longipes Acanthoplus discoidalis Acanthoproctus diadematus Enyaliopsis sp. Spalacomimus liberiana Listroscelidinae: Requenini Requena verticalis Meconematinae Supersonus spp. Phlugis spp. Meconema thalassinum Meconema meridionale Mecopodinae Mecopoda elongata Phaneropterinae: Ephippithytae Caedicia simplex Polichne sp. Phaneropterinae: Barbitistini Ancistrura nigrovittata Leptophyes punctatissima Leoptophyes albovittata Isophya pyrenaea Isophya modestior CA sensilla 23 15 26 2a 28 28 3541 Males: 34+1 Females: 34+2 35+1 Males: 32+1 Females: 33+1 3241 3441 33 Males: 33+1 Females: 32 3241 20 24+1 31 55 12-14 12-14 21 16 15 4842 45 35 32 37 2841 24 22 22 27 3442 Tympana covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered covered open open covered open covered covered covered, tympanal slits asymmetrical open tympana open open open open open open open open open open JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) Reference O. S. Korsunovskaya, personal communication Zhantiev et al. 1995 Knetsch 1939, Schumacher 1979 Schumacher 1979 Fullard et al. 1989 Montealegre-Z et al. 2012 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Strauf et al. 2017 Oldfield 1984 Kalmring et al. 1995b Knetsch 1939 Schumacher 1979 Rossler 1992b Lakes and Schikorski 1990 Lakes and Schikorski 1990 Kowalski and Lakes-Harlan 2013 Kowalski and Lakes-Harlan 2013 Kowalski and Lakes-Harlan 2013 Kowalski and Lakes-Harlan 2013 Kowalski and Lakes-Harlan 2013 Romer et al. 1998 Satria-S et al. 2014, F Montealegre-Z, personal communication FE. Montealegre-Z, personal communication Knetsch 1939 Schumacher 1973 Schumacher 1979 Strauf et al. 2012 Hummel et al. 2017 Oldfield 1982 Oldfield 1984 Ostrowski and Stumpner 2010 Rossler et al. 1994 Knetsch 1939 Schumacher 1973 Knetsch 1939 Knetsch 1939 Strauf et al. 2014 210 J. STRAUR Table 1. (Continued). Species CA sensilla Tympana Reference Poecilimon ornatus 3841 open Straus et al. 2014 Poecilimon gracilis 3441 open Strauf et al. 2014 Poecilimon elegans 3241 open Strauf et al. 2014 Poecilimon chopardi 30+1 open Strauf et al. 2014 Poecilimon intermedius 1741 open Lehmann et al. 2007 Poecilimon ampliatus 21+1 open Lehmann et al. 2007 Polysarcus denticauda 49+2 open Sickmann et al. 1997 Phaneropterinae: Holochlorini Ancylecha fenestrata Males: 116 (md) Females: 86 (md) Phaneropterinae: Phaneropterini Phaneroptera falcata 39 Phaneropterinae: Steirodontini Stilpnochlora couloniana 45-55 Phasmodinae Phasmodes ranatriformis 16-18 Pseudophyllinae Nastonotus foreli 22 Tettigoniinae: Decticini Decticus verrucivorus 3341 Decticus albifrons 34+1 Tettigoniinae: Gampsocleidini Gampsocleis gratiosa 3341 Tettigoniinae: Tettigoniini Tettigonia viridissima 37 3641 Tettigonia cantans Ja41 Tettigoniinae: Platycleidini Bicolorana bicolor 23 Metrioptera roeselii 26 Metrioptera brachyptera 24 Platycleis albopunctata (syn. denticulata) 23 Psorodonotus illyricus 3141 Tettigoniinae: Pholidopterini Pholidoptera griseoaptera 24+1 Zaprochilinae Kawanaphila nartee 18+1 This becomes apparent in comparison to the crickets, the other ensiferan group studied in detail for the neurobiological substrate for hearing (Pollack and Hedwig 2017), where the tympanal or- gan anatomy has been analysed mainly for a few selected model species (summary: Ball et al. 1989): Gryllus bimaculatus, Gryllus campestris (Michel 1974, Eibl 1978), Achaeta domesticus (Schwabe 1906), Teleogryllus commodus (Klose 1996), several Eneopterinae species (Schneider et al. 2017), and the mogoplistine Cycloptiloides canariensis with a unique hearing organ (Michel 1979). The re- search on diverse tettigoniid lineages not only addressed the neu- rophysiology of sound processing, but also led to the study of the effects of species divergence, the differences in the communication system, and the evolutionary regression of the hearing organs on the structure of the CA. Functional and evolutionary factors influencing the sensil- lum numbers in the crista acustica The sense of hearing provides important adaptations for mate recognition and localization as well as predator (bat) detection. Such positive selection for hearing will result in well-developed hearing organs with auditory receptors detecting frequency ranges of both intraspecific calls and ultrasonic frequencies of bats. How- Scherberich et al. 2017 Kowalski 2010 anterior covered, posterior open open Schumacher 1973 open Lakes-Harlan and Scherberich 2015 no tympanum Lakes-Harlan et al. 1991 covered FE. Montealegre-Z, personal communication covered Roéssler and Kalmring 1994 covered Rossler and Kalmring 1994 covered Lin et al. 1994 covered Schumacher 1973 Kalmring et al. 1995a covered Kalmring et al. 1995a covered Schumacher 1973 Kowalski 2010 covered Knetsch 1939, Schumacher 1979 covered Schumacher 1973 covered Kalmring et al. 1995b covered Rossler et al. 1994 open Bailey and Romer 1991, Rentz 1993 ever, additional factors could affect the structure of the hearing organs, like genetic drift, allometry, and phylogenetic constraints (structures preserving the ancestral state) as well as physical con- straints (see Strauf$ and Stumpner 2015 for tympanal organs in general). From the comparative data, it can be concluded that CA under sexual and natural selection usually contain 22-50 sensilla, with most species having 25-40 auditory sensilla. These numbers thus appear to be adequate and adaptive to allow sound detection, frequency resolution, intensity discrimination, and input to the CNS for directional and temporal analysis, though smaller num- bers do not necessarily exclude these physiological functions. For example, Meconema thalassinum does not use tegminal stridulation and has a low number of 16 auditory sensilla (Schumacher 1973, 1979), and in the tympanal hearing organ of this species, travel- ling waves were recorded over the CA that indicate frequency anal- ysis (FE Montealegre-Z, personal communication). As both higher and lower numbers from the most common numbers are found, the evolutionary events behind the extreme values can be analyzed based on this comparative background. In addition, functional and physiological data are required to characterize the changes in the sensory organs further. Below, the different evolutionary forces are discussed for the CA, with expected outcomes of the effect of selection. Neutral evolution (drift) is difficult to support directly JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS by comparing anatomical traits or physiological features, as it is supported by the lack of evidence for explanations based on adap- tions or constraints if detailed information on the genetic poly- morphisms that encode a trait is not available (Schul et al. 2014). It likely contributes to the regression of auditory systems if a selec- tion pressure ceases (e.g., Lakes-Harlan et al. 1991, Lehmann et al. 2007, Strauf$ and Stumpner 2015). Evolutionary regression in the hearing organ.—Strong evidence for the role of selection pressures on the tympanal organs can be ob- tained from species where either natural or sexual selection have ceased. In these cases, often a regression is noted that can reduce the size of spiracles of the acoustic trachea, and potentially also the number of auditory sensilla. Such regression could be due to neutral evolution (drift) after selection ceases to maintain a cer- tain structure, or auditory sensilla could be selected against, as they require energy to develop and maintain (see e.g., Laughlin et al. 1998). Case studies under which conditions and to what extent such regressions occur are discussed below. Sexual dimorphism: Australian Kawanaphila show a notable sex- ual dimorphism in the auditory system, with a smaller auditory spiracle in males than in females and also smaller acoustic bulla in the prothorax (Bailey and ROmer 1991, Mason and Bailey 1998). Three species in the genus have been studied, revealing a gradi- ent in the reduction of the acoustic spiracle. While in Kawanaphila yarraga the auditory spiracle in males is significantly smaller than in females, in males of K. nartee and K. mirla no external auditory spiracle is developed, and males thus show decreased auditory sen- sitivity compared to females (Bailey and Romer 1991, Mason and Bailey 1998). Blocking the auditory spiracle in K. nartee females re- sulted in a reduced sensitivity similar to conspecific males (Bailey and Romer 1991). The number of CA sensilla in K. nartee males and females is not different between sexes, with 18 + 1 sensory neurons (Bailey and ROmer 1991). The CA of the other Kawanaphila species has not been studied for the number of sensilla, and such data might complement the evidence for gradual regression in these species. The auditory behavior of males also differs, with decreased male competition in K. mirla that is acoustically mediated between callers as indicated by lower distances between males (Mason and Bailey 1998) to the absence of any auditory behavior in male K. nartee (Bailey and Simmons 1991). This gradual decrease in the auditory function of males from different species and intraspecific dimorphism indicate that the male hearing organ is the result of an evolutionary regression from a well-developed auditory system. Since in K. mirla the regression is already anatomically and physi- ologically detectable, while auditory behavior of male-male com- petition still occurs, the decline in hearing function seems not to have triggered the regression (Mason and Bailey 1998). Mimesis: A further reduction is found in the Australian stick ka- tydid, Phasmodes ranatriformis. These mimetic animals remarkably resemble stick insects, and do not produce acoustic signals (Rentz 1993), resulting in a weakened selection pressure for hearing. Spir- acles are small and tympana are only weakly expressed in males and females as depressions with thinner leg cuticle (Lakes-Harlan et al. 1991, Rentz 1993). The CA is present in the legs of females and males with 16-18 sensilla in the foreleg (Lakes-Harlan et al. 1991), also indicating a low elaboration of the auditory sense. Parthenogenesis: In tettigoniids, parthenogenesis (loss of males) is rare but presents an interesting evolutionary scenario, since 211 selection for intraspecific signal detection ceases without males producing acoustic signals. In Poecilimon intermedius, an obligate parthenogenetic species, only females occur (Lehmann et al. 2011) and the number of auditory sensilla is very low at 17 + 1, even lower than in the sister species P. ampliatus (21 + 1). This indicates an evolutionary regression of the hearing organ, while selection pressure from predators may have maintained some hearing func- tion (Lehmann et al. 2007). Change of signalling behavior: In two Meconema species, acoustic signals are not produced by tegminal stridulation as males of M. thalassinum and M. meridionale produce sound and likely vibration signals by tapping or drumming with the hind leg on the substrate (Sismondo 1980, Vahed 1996, Ingrisch and Rentz 2009). In these species with open tympana, the number of auditory sensilla is very low at 15 (M. meridionale) and 16 (M. thalassinum) sensilla (Schu- macher 1979). However, the CA in M. thalassinum expresses travel- ling waves, indicating functional hearing (FE Montealegre-Z, personal communication). Female bush crickets of certain species can also use vibrational signals produced during wing stridulation for orientation toward males over shorter distances (Ephippiger ephippiger: Stiedl and Kalmring 1989). Since the most sensitive vibration receptor in the tibia is the subgenual organ (Fig. 1C), the tapping may also affect the signal detection by both auditory and vibratory sensilla, initiat- ing a regressive process of the CA. However, since neuroanatomical data from related species with tegminal stridulation species are not available, the degree of regression is unclear in this case. Notably, even lower numbers of CA sensilla are also found in meconematine species with ultrasonic calls by tegminal stridulation (12-14 sensilla, Table 1; EF Montealegre-Z, personal communication). Influence of the communication system on the auditory system.—De- pending on the communication system, different selective require- ments can also differentially affect the auditory organs between the sexes. In Phaneropterinae, acoustic duets are most common (Heller et al. 2015), and the auditory behaviour has been studied in detail in the genus Poecilimon (Heller and von Helversen 1986, 1993, Heller 1990). The communication system in most species is bidirectional with male calls, and softer and short female replies (Heller and von Helversen 1986, Heller et al. 1997b, von Helvers- en et al. 2015). For the detection of the female replies, males should be selected for higher auditory sensitivity, morphological- ly reflected in larger spiracles to amplify the sound. In addition, males could benefit from summation of more sensilla to detect the soft and short female responses. In Poecilimon, the bidirection- al communication system is also the evolutionary ancestral state for the group (see Heller 1990). However, in three distinct line- ages the female reply was abolished (in the P. ampliatus group, the P. propinquus group, and in P. jablanicensis of the P. ornatus group), resulting in a secondary unidirectional communication system in which males should no longer be selected for higher auditory sensitivity. Testing for the possible correlation between the audi- tory system and the communication system showed the expected correlation of spiracle sizes with the communication system, with consistently larger spiracles in bidirectional signalling species. In addition, spiracles in males of these species are larger than in con- specific females, supporting the influence of sexual selection for higher male hearing sensitivity. Spiracle sizes in unidirectionally signalling species are smaller but show no sex-specific differences in spiracle size. The expected higher number of auditory sensilla was found in species with a bidirectional communication system (32-38 sensilla), with a strong relationship to body size (allome- JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 212 try, see also below). Notably, the sensillum numbers in P. chopardi (P. propinquus group) are only slightly lower (at 29 sensilla), while in species of the P. ampliatus group, they are ~30% lower than the correlation to body size would indicate (decreased to 17-21 sensilla) and with similar smaller spiracle sizes in both groups (StraufS et al. 2014). Thus, representatives in the groups with a secondary unidirectional signalling show evidence for an evolu- tionary regression in the auditory structures. These differences in Poecilimon auditory sensilla are the greatest variation between tet- tigoniid species from the same genus known so far, highlighting the evolutionary changes in the Poecilimon auditory system and the importance of sexual selection. It is uncertain why the degree of sensilla regression differs between members of the P. ampliatus and propinquus group. Further, it is difficult to identify the evolu- tionary starting point for the regression—if this started with the loss of the female reply reducing the selection for high sensitivity (larger spiracles) or if a reduced spiracle size led to a lower au- ditory sensitivity and the loss of female responses (Strauf et al. 2014). The evolutionary shift from bidirectional to unidirectional communication may depend on the mating success of females in relatively high population densities (P. ampliatus: von Helversen et al. 2012), the active distance between the mates, and the effec- tive range of the acoustic signalling system (von Helversen et al. 2015). Here, the complexity of the acoustic environment is im- portant as well, including the role of background noise (R6Omer and Bailey 1998), signal transmission (ROmer 2016), and natu- ral selection by predators that may maintain the hearing organs (Lehmann et al. 2007). Does a correlation exist between carrier frequency of the communication signal and CA design?.—Tettigoniid tympanal organs are broadly tuned (Kalmring et al. 1990, Réssler and Kalmring 1994, Rossler et al. 1994). So far, a general correlation between spectral char- acteristics of the intraspecific signals and the number of auditory sensilla has been difficult to identify (Réssler et al. 2006): while the sensitivity of the auditory organ results from the summed ac- tivity of the CA sensilla and structures like the spiracles and bullae, similar tuning of receptors from different species or the absolute auditory sensitivity are not dependent on the overall number of CA sensilla (Réssler and Kalmring 1994, Scherberich et al. 2017). A change in carrier frequency of calls might affect the tuning of sensilla in the hearing organ, rather than the overall number of auditory sensilla. However, to detect extremely short female re- plies in duets, an increased number of auditory sensilla activated simultaneously could benefit the signal detection (see below for the auditory fovea). Auditory sensilla with highly similar frequency tuning were found despite significant differences in the CA length and num- ber of CA sensilla, both in related species (Kalmring et al. 1992) and also in more distantly related species (Kalmring et al. 1995b). Physiological data from some other species, however, showed specific hearing tuning for individual sensilla that adapt the fre- quency range to intraspecific call frequencies by broadening (Neoconocephalus bivocatus: H6bel and Schul 2007) or narrowing (Ancylecha fenestrata: Scherberich et al. 2016) the frequency re- sponse. The tonotopic organization of sensilla also contributes to intensity coding as stimuli at higher amplitudes activate both the sensilla tuned to the specific stimulus frequency together with sen- silla tuned to other best frequencies that are also activated at in- creased amplitudes due to their broad tuning ranges (ROmer et al. 1998, Hennig et al. 2004, Hébel and Schul 2007, Stumpner and Nowotny 2014). Whether such recruitment at higher amplitudes J. STRAUS could affect the hearing organ to extend the set of auditory sensilla significantly is so far unclear. Currently, the frequency representation over the CA is char- acterized only for a few species. The relative proportions of low vs. high frequency receptors differ along the CA, however, and are often adapted to the main frequency of calls by a relatively higher proportion of sensilla tuned to conspecific call frequen- cies (Kalmring et al. 1990, 1993, Rossler et al. 2006). This was shown by Current Source Density (CSD) analysis using a multi- unit electrode system to record neuronal ensemble activities of sensory afferents in the auditory neuropile by their field potentials in relation to stimuli of different frequencies (Breckow et al. 1982, Rossler et al. 1990). However, this correlation so far provides no direct explanation for why a specific number of CA sensilla evolved in a given species. In Neoconocephalus, the number of CA sensilla from nine species was statistically negatively correlated to the species’ call frequency (Strauf% et al. 2017). Since this correla- tion was also found for the CA length and body size, it was as- sumed to indicate an allometric relationship (see below), because larger animals have larger stridulatory structures that produce calls in lower frequencies, and body size also influences the number of CA sensilla and CA length. Frequency representation in an auditory fovea: The auditory fo- vea is an adaptation of frequency representation by highly similar tuning of multiple adjacent CA sensilla. In this case, frequency tun- ing is not linearly graded over the CA length. For the duetting phan- eropterine Ancylecha fenestrata, a remarkable sexual dimorphism was shown where the ears of males contain 35% more auditory sensilla (median: 116) compared to females (86), and also a longer CA (Scherberich et al. 2016, 2017). Irrespective of the difference be- tween sexes, this is the highest number of CA sensilla reported so far (Table 1). Physiologically, their CA shows an interrupted gradient in frequency tuning with a central region of 55 sensilla, where the change in characteristic frequency is less steep than at the proximal and distal CA ends. These sensilla in males are tuned to the domi- nant frequency of the female acoustic reply to male calls at about 10 kHz, and thus mediate the male phonotaxis. Females respond to male calls with a single, short sound of 42 ms duration (median; Scherberich et al. 2016). The auditory fovea can contribute to direc- tional hearing of the very short and rare female response signals, as population coding from increased numbers of afferents improves the processing of temporal and intensity interaural differences at interneuron level to locate a sound source more reliably (Scher- berich et al. 2017). The tuning of the auditory fovea also concurs in morphology with a CA region of similar organ height that does not follow the curvature of the CA surface (Scherberich et al. 2017). This organization is a sex-specific (male) adaptation relating to the specific duetting communication and indicates a strong sexual se- lection for detecting the signals of potential mates and shows most clearly an adaptive increase in auditory sensilla. Similar functional organizations with adjacent sensilla tuned to the same characteris- tic frequency are also found in CAs with less sensilla (< 30; Oldfield 1985, Montealegre-Z et al. 2012), but by far not as strong as in the case of A. fenestrata—this is the only case of a tettigoniid hearing organ with over 100 auditory sensilla known so far. Adaptive significance for CA changes as a result of temporal call pat- tern.—The recognition of call patterns is carried out by the central nervous system, while the auditory sensilla code the temporal/ syllable pattern (Schul and Rossler 1993, Pollack 1998). Hence, differences in call patterns are not expected to be a major influ- JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS ence on CA sensilla. One possible exception is the signal duration, which in cases of short acoustic signals would benefit from more sensilla that provide stronger input to the CNS (see the above dis- cussion on the auditory fovea). The North American genus Neoconocephalus is a study model for the evolutionary diversification of call patterns and their rec- ognition mechanisms (Schul et al. 2014). Among tettigoniids, the male Neoconocephalus calls have notably narrow frequency bands with center frequencies mainly at 10-15 kHz (Schul and Patterson 2003). The ancestral call pattern in Neoconocephalus is characterized by continuous calls with single pulses at fast repeti- tion rates (Schul et al. 2014). During the evolutionary radiation of the group, the call patterns diversified repeatedly into discon- tinuous calls, slow repetition rates, and/or double pulses (Schul et al. 2014). The evolutionary diversification is highlighted e.g., by the repeated evolution of double-pulsed calls (Schul et al. 2014, Frederick and Schul 2016). Studying the CA anatomy of nine spe- cies representing different taxonomic groups, life histories, call patterns, and call center frequencies, similar averages from 32-35 sensilla between the species were documented (Strauf et al. 2017). A similar number of 35 sensilla is found in the most closely re- lated Ruspolia (R. nitidula, Schumacher 1979), suggesting that the ancestral Neoconocephalus already had a number of auditory sen- silla in these ranges. The variation between Neoconocephalus spe- cies was influenced by the species specificity as well as body size (allometry), but not by phylogenetic relationships. Statistical analysis for standardized effects of the call pattern also revealed correlations with CA sensillum numbers and CA length (Fig. 2). Male calls with slow pulse rates correlated with significantly more CA sensilla and longer CA (Fig. 2A), continu- ous calls with the increased number of CA sensilla (Fig. 2B), and double pulses with a longer CA (Fig. 2C). In the latter case, dou- ble pulsed calls also correlate with a higher number of sensilla, though the increase was not statistically significant. These correla- tions indicate a clear influence of sexual selection on the CA. The findings are notable since the analysis of temporal call pat- terns is not carried out by the sensilla but in the central nervous sys- tem. The increased number of sensilla in species with slow-calling rates may be most easy to explain, as they could be an adaptation to shorter signals by providing a relatively stronger input to the CNS by additional sensilla. In addition, indirect effects of acoustic signalling on the CA are likely (Strauf et al. 2017). The correlation of discontinuous calls with lower sensillum numbers may depend on the behavioral ecology of signallers since discontinuously call- ing species have higher population densities (Greenfield 1990), which in turn may relax the selection on the auditory system. A continuously calling species (N. affinis) occurring in relatively high population densities (Greenfield 1983) also had relatively low CA sensilla (Strauf et al. 2017). Notably, not all evolutionary-derived call patterns in Neoconocephalus correlate to the increased number of CA sensilla (Fig. 2). While the differences in CA sensilla be- tween Neoconocephalus species are small compared to those found in Poecilimon, the evolution of call patterns and call recognition mechanisms triggered the recent radiation of the group (Schul et al. 2014) and the hearing organs might diverge further in response. Allometry.—Allometry refers to the relation of a structure to body size. It can highlight the influence of selection between body size and a morphological character under investigation, inferred from positive allometry and low morphological variation in the charac- ter (see also Bailey and Kamien 2001 for sound transmitting struc- tures and Anichini et al. 2017 for stridulatory structures). Hence, a 213 a [355 CA sensilla [JCA length 900 2 = 750 — W) 5 é Ww) = < 600 5 O 3. 450 single pulse double pulse Pulse pattern Fig. 2. Standardized effects of call patterns in Neoconocephalus on the number of CA sensilla and CA length for A. Pulse rate; B. Struc- ture of continuous or discontinuous calls; and C. Pulse pattern. The evolutionary derived call characters are a slow pulse rate, dis- continuous calls, and double pulses. Significance levels: * 0.05 > p > 0.01; ** 0.01 > p > 0.001. Adapted from Straufs et al. 2017, with permission from John Wiley and Sons. JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 214 larger body size would predict a longer CA and/or a higher number of auditory sensilla. Different features in the tettigoniid auditory system, like the spiracle and tracheal bulla size, were shown to be determined by allometry (Bailey 1998, Bailey and Kamien 2001). If larger individuals have larger spiracles they are more sensitive, that sensitivity can be determined by allometric relationships (Requena verticalis: Bailey 1998, but see also ROmer et al. 2008 with a broader species sampling). The correlation of auditory sensillum numbers to body size was first suggested by Knetsch (1939), albeit with lim- ited data from nine species and diverse genera. Closely related spe- cies were analyzed for Poecilimon (Strauf$ et al. 2014) and Neocono- cephalus (Strauf$ et al. 2017) with a substantial influence of body size found on the CA for both groups, but evolutionary changes were also detected that affected the sensillum numbers more strongly: the reduction of acoustic signalling as well as adaptations to temporal call features such as the pulse rate, pulse pattern, and call structure can override the allometric relationship (see above). Allometry is thus one among several factors influencing the CA. Different traits have been used as a measure for body size, such as the body length (Knetsch 1939), pronotum length (Bailey 1998, Bailey and Kamien 2001), hind femur length (Lehmann 1998, Bai- ley and Kamien 2001, Schul and Patterson 2003, Strauf et al. 2014, Anichini et al. 2017), or foreleg tibia length (Knetsch 1939). As shown for R. verticalis, hind femur and pronotum length are not isometrically related (Bailey and Kamien 2001), and the choice of anatomical parameter(s) to measure allometry is important. Phylogenetic ancestral states. —Phylogenetic constraints result in a re- tained character state in successively evolving species. Constraints would set limits on the evolutionary changes in a character and counter the influence of selection pressures, retaining an ances- tral situation. For the CA, the studies including outgroups found both cases were specific adaptations (Neoconocephalus: Straufs et al. 2017) and regressive changes (Poecilimon: Strauf% et al. 2014) indicate the importance of sexual selection for elaborate CAs and argue against a phylogenetic constraint on sensillum numbers in these taxa. Certainly, further comparative studies including mul- tiple species and outgroup species will give more insights on the adaptive significance of sensillum numbers. A neuroanatomical feature that was discussed as a possible ancestral state are the distally concentrated sensilla in the CA of Polysarcus denticauda, leading to pairs or triplets of somata (Sick- mann et al. 1997) and a loss of frequency resolution for frequen- cies above 20 kHz in these sensilla (Kalmring et al. 1996). Such a crowded organization of somata and dendrites was also found in several species of Phaneropterinae with thin tympana and a vari- able number of sensilla (Strauf$ et al. 2012), which makes an an- cestral situation in P. denticauda less likely. Relation to tympanum structure.—It has been noted that species with open tympana often have higher numbers of auditory sensilla (Lakes and Schikorski 1990). For example, Mecopoda elongata and Polysarcus denticauda have close to 50 CA sensilla and open tym- pana. P. denticauda is also exceptional as it has very thick tympana (Sickmann et al. 1997). Supersonus spp. have narrow asymmetric slits (Sarria-S et al. 2014) and exceptionally few CA sensilla with 12-14 (FE Montealegre-Z, personal communication). However, notable exceptions for this relationship between CA sensilla and tympanum morphology exist, as one of the species with the lowest known sensillum numbers has open tympana (Phlugis spp.) and the species with the highest known sensillum number (Ancylecha fenestrata) has a cover at the anterior tympanum. Specific evolu- J. STRAUS tionary scenarios for increasing or decreasing sensillum numbers obviously override a possible relation with the tympanum mor- phology in these cases. Diversity of tettigoniid auditory organs and evolutionary causes With respect to the number of CA sensilla, only a small fraction of the tettigoniid species has been studied so far. Neuroanatomical and physiological studies have revealed a diversity in the number of auditory sensilla among tettigoniid species that is species-specif- ic. To characterize the auditory system of any species, the number of CA sensilla is an important parameter, together with tympanal and tracheal dimensions and the hearing threshold curve. So far, the tonotopic organization of the CA has been studied in even fewer species, and it remains to be analyzed how the changes in neuron numbers affect frequency representation and the accuracy of frequency discrimination (Réssler and Kalmring 1994). Obvi- ously, the auditory system consists of successive levels of signal analysis in the central nervous system, and further processing in the auditory pathway may increase or decrease the relevance of specific cues for the receiver (e.g., Stumpner and Nowotny 2014). While comparative studies indicate divergences in the num- ber of CA sensilla between species, it is so far easier to explain such divergence in adding or reducing sensilla than to explain the functional requirements which determine a certain number of sensilla in a specific species. Such cases of divergence indicate the importance of multiple determinants. The elaborate auditory system of Tettigoniidae is formed by several selective forces: natu- ral and sexual selection as well as allometry (Stumpner and von Helversen 2001, Robinson and Hall 2002, Straufs and Stumpner 2015), which makes it more difficult to analyze the contribution of specific influences. For a tympanal organ that is shaped by sex- ual and natural selection, it is somewhat difficult to determine the lower end of sensillum numbers since some species which show no regressive elements have numbers such as 24 sensilla (Myga- lopsis, Pholidoptera) or 22 sensilla (Requena verticalis, Nastonotus foreli). Poecilimon ampliatus with 21 sensilla, compared to related species from the genus, shows evidence for regression both for the spiracles and the CA sensilla. This highlights the importance of a comparative approach covering several species. However, the strong influence of sexual selection even at the level of the CA sensilla can be detected for several model groups (Lehmann et al. 2007, Strauf et al. 2017). Based on the currently available knowledge, some groups of tettigoniids are promising candidates for further studies of neuro- anatomy and the functional morphology of the CA: For the large group of Pseudophyllinae with over 1000 species, important phys- iological experiments have shown ultrasonic call frequencies and directional hearing mediated by tympanal slits rather than sound input via the small spiracles (Mason et al. 1991), but the CA is so far only rarely studied (see Nastonotus foreli, Table 1). A detailed analysis of the CA for such species with ultrasonic carrier frequencies of calls (Morris et al. 1994, Montealegre-Z et al. 2006) will be important to study the CA frequency representation. For the Australian K. nartee, which produces narrow ultrasonic calls, the number of sensilla is rather low at 18 CA sensilla (Gwyn- ne and Bailey 1988, Bailey and ROmer 1991). Remarkably, spe- cies calling at ultrasonic frequency ranges can have an even lower number of CA sensilla (Supersonus: 12-14 sensilla; F. Montealegre- Z, personal communication), inviting further investigations and functional comparisons. JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS Biomechanical analysis in Onomarchus uninotatus (Pseudo- phyllinae) showed fascinating adaptations for the two tympanal membranes with differential tympanal tuning (acoustic partition- ing) of the anterior tympanum as a low-pass filter and the poste- rior tympanum as a high-pass filter (Rajaraman et al. 2013). The structure and mechanics of the CA and associated elements would be interesting for their organization in this case. Further work on already researched groups will extend the understanding of evolutionary changes in the CA. For example, in the genus Poecilimon, the CA anatomy of relatively few spe- cies is known. Additional data are relevant from those species already studied with respect to auditory physiology (P. laevis- simus, P. thessalicus: Stumpner and Heller 1992), hearing organ embryology (P. affinis: Meier and Reichert 1990), or the acoustic communication system (unidirectional signalling in the P. pro- pinquus group, and further bidirectional species of the P. ornatus group and the unidicrectional P. jablanicensis: Chobanov and Heller 2010) to better understand auditory adaptations and di- versification in the CA. Finally, allometry in the CA is worth exploring in more detail, both within and between species. For tettigoniids, the influence of allometry on CA sensilla is not studied in detail for intraspecific variation, which would be interesting to address for different com- munication systems and the influence of selection. For studies on the auditory system of additional tettigoniid species, the question of what determines the number of auditory sensilla can guide the analysis of the hearing organ and can also be expected to give in- sights relevant to sensory evolution. Acknowledgements I wish to thank Gerlind Lehmann and Karim Vahed for in- viting a contribution to the symposium “Sexual selection in the Orthoptera” at the 13" International Congress of Orthopterology from which this review originated. I am thankful to Olga S. Kor- sunovskaya for sharing information on the CA in Bradyporinae and to Fernando Montealegre-Z for sharing information on the CA in Pseudophyllinae and Meconematinae, and for discussions. I thank NataSa Stritih Peljhan for thoughtful comments on an ear- lier version of the manuscript. I wish to thank two reviewers for their insightful and constructive comments. I am indebted to Ku- mar Chowdhury for the linguistic corrections. References Anichini M, Kuchenreuther S, Lehmann GUC (2017) Allometry of male sound-producing structures indicates sexual selection on wing size and stridulatory teeth density in a bushcricket. Journal of Zoology 301: 271-279. https://doi.org/10.1111/jzo.12419 Baden T, Hedwig B (2010) Primary afferent depolarization and fre- quency processing in auditory afferents. The Journal of Neuro- sciences 30: 14862-14869. https://doi.org/10.1523/JNEURO- SCI.2734-10.2010 Bailey WJ (1985) Acoustic cues for female choice in bushcrickets (Tetti- goniidae). In: Kalmring K, Elsner N (Eds) Acoustic and Vibrational Communication in Insects. Parey, Hamburg, 101-110. Bailey WJ (1990) The ear of the bushcricket. In: Bailey WJ, Rentz DCF (Eds) The Tettigoniidae: Biology, Systematics and Evolution. Craw- ford House Press, Bathurst, 217-247. https://doi.org/10.1007/978-3- 662-02592-5_12 Bailey WJ (1991) The Acoustic Behaviour of Insects. An Evolutionary Per- spective. Chapman and Hall, London, 226 pp. Bailey WJ (1993) The tettigoniid (Orthoptera: Tettigoniidae) ear: Multiple functions and structural diversity. International Journal of Insect Mor- 215 phology and Embryology 22: 185-205. https://doi.org/10.1016/0020- 7322(93)90009-P Bailey WJ (1998) Do large bushcrickets have more sensitive ears? Natu- ral variation in hearing thresholds within populations of the bush- cricket Requena verticalis (Listroscelidinae: Tettigoniidae). Physi- ological Entomology 23: 105-112. https://doi.org/10.1046/j.1365- 3032.1998.232071.x Bailey WJ (2003) Insect duets: Underlying mechanisms and their evolu- tion. Ecological Entomology 28: 157-174. https://doi.org/10.1046/ j.1365-3032.2003.00337.x Bailey W, Kamien D (2001) Hearing dimorphism, trait variation and con- flicts over space in the thorax of the bushcricket Requena verticalis (Listroscelidinae: Tettigoniidae: Orthoptera). Journal of Comparative Physiology A 187: 647-652. https://doi.org/10.1007/s003590100236 Bailey WJ, Romer H (1991) Sexual differences in auditory sensitivity: Mismatch of hearing threshold and call frequency in a tettigoniid (Orthoptera, Tettigoniidae: Zaprochilinae). Journal of Comparative Physiology A 169: 349-353. https://doi.org/10.1007/BF00206999 Bailey WJ, Simmons LW (1991) Male-male interactions and sexual dimor- phism in the ear of a zaprochiline tettigoniid. Journal of Insect Behav- ior 4:51-64. https://doi.org/10.1007/BF01092551 Bailey WJ, Stephen RO (1978) Directionality and auditory slit function: A theory of hearing in bushcrickets. Science 201: 633-634. https://doi. org/10.1126/science.201.4356.633 Ball EE, Oldfield BP, Michel Rudolph K (1989) Auditory organ structure, development, and function. In: Huber EF Moore TE, Loher W (Eds) Cricket Behavior and Neurobiology. Ithaca, Comstock Publishing As- sociates, 391-422. https://doi.org/10.7591/9781501745904-015 Belwood JJ (1990) Anti-predator defences and ecology of neotropical forest katydids, especially the Pseudophyllinae. In: Bailey WJ, Rentz DCF (Eds) The Tettigoniidae: Biology, Systematics and Evolution. Crawford House Press, Bathurst, 8-26. https://doi.org/10.1007/978-3-662-02592-5_2 Breckow J, Kalmring K, Eckhorn E (1982) Multichannel-recordings and real-time current source density (CSD) analysis in the central-nervous system of insects. Problems and methods of application. Biological Cybernetics 45: 115-121. https://doi.org/10.1007/BF00335238 Chobanov DP, Heller K-G (2010) Revision of the Poecilimon ornatus group (Orthoptera: Phaneropteridae) with particular reference to the taxa in Bulgaria and Macedonia. European Journal of Entomology 107: 647-672. https://doi.org/10.14411/eje.2010.073 Eibl E (1978) Morphology of the sense organs in the proximal tibia of Gryllus campestris L. and Gryllus bimaculatus deGeer (Insecta, Ensfera). Zoomorphology 89: 185-205. https://doi.org/10.1007/BF00993947 Faure PA, Hoy RR (2000) The sounds of silence: Cessation of singing and song pausing are ultrasound-induced acoustic startle behaviors in the katydid Neoconocephalus ensiger (Orthoptera; Tettigoniidae). Journal of Comparative Physiology A 186: 129-142. https://doi.org/10.1007/ s003590050013 Frederick K, Schul J (2016) Character state reconstruction of call diversity in the Neoconocephalus katydids reveals high levels of convergence. PLoS Currents Tree of Life. Edition 1. https://doi.org/10.1371/cur- rents.tol.0c5d76728d73ef9c3dbe8065f70ea4cb Friedrich H (1927) Untersuchungen tiber die tibialen Sinnesapparate in den mittleren und hinteren Extremitaten von Locustiden. I. Zoologis- cher Anzeiger 73: 42-48. Friedrich H (1928) Untersuchungen iiber die tibialen Sinnesapparate in den mittleren und hinteren Extremitaten von Locustiden. II. Zoolo- gischer Anzeiger 75: 86-94. Fullard JH, Morris GK, Mason AC (1989) Auditory processing in the black-sided meadow katydid Conocephalus nigropleurum (Orthoptera: Tettigoniidae). Journal of Comparative Physiology A 164: 501-512. https://doi.org/10.1007/BF00610444 Fullard JH, Yack JE (1993) The evolutionary biology of insect hear- ing. Trends in Ecology and Evolution 8: 248-252. https://doi. org/10.1016/0169-5347(93)90200-9 Greenfield MD (1983) Unsynchronized chorusing in the coneheaded ka- tydid Neoconocephalus affinis (Beauvois). Animal Behaviour 31: 102- 112. https://doi.org/10.1016/S0003-3472(83)80178-X JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 216 Greenfield MD (1990) Evolution of acoustic communication in the ge- nus Neoconocephalus: discontinuous songs, synchrony, and interspe- cific interaction. In: Bailey WJ, Rentz DCF (Eds) The Tettigoniidae: Biology, Systematics and Evolution. Crawford House Press, Bathurst, 72-97. https://doi.org/10.1007/978-3-662-02592-5_5 Greenfield MD (2016) Evolution of acoustic communication in insects. In: Pollack GS, Mason AC, Popper AN, Fay RR (Eds) Insect hearing. Springer International, Cham, 17-47. https://doi.org/10.1007/978-3- 319-28890-1_2 Gwynne DT (2001) Katydids and Bushcrickets: Reproductive Behavior and Evolution of the Tettigoniidae. Comstock, Ithaca, 317 pp. Gwynne DT, Bailey WJ (1988) Mating systems, mate choice and ultrasonic calling in a zaprochiline katydid (Orthoptera: Tettigoniidae). Behav- iour 105: 202-223. https://doi.org/10.1163/156853988X00025 Heinrich R, Jatho M, Kalmring K (1993) Acoustic transmission charac- teristics of the tympanal tracheae of bushcrickets (Tettigoniidae). II: Comparative studies of the tracheae of seven species. Journal of the Acoustical Society of America 93: 3481-3489. https://doi. org/10.1121/1.405678 Heller K-G (1990) Evolution of song pattern in East Mediterranean Phan- eropterinae: Constraints by the communication system. In: Bailey WJ, Rentz DCF (Eds) The Tettigoniidae: Biology, Systematics and Evolution. Crawford House Press, Bathurst, 130-151. https://doi. org/10.1007/978-3-662-02592-5_8 Heller K-G, Hemp C, Ingrisch S, Liu C (2015) Acoustic communication in Phaneropterinae (Tettigonioidea) - A global review with some new data. Journal of Orthoptera Research 24: 7-18. https://doi. org/10.1665/034.024.0103 Heller K-G, Schul J, Ingrisch S (1997a) Sex-specific differences in song fre- quency and tuning of the ears in some duetting bushcrickets (Orthop- tera: Tettigonioidea: Phaneropteridae). Zoology 100: 110-118. Heller K-G, von Helversen D (1986) Acoustic communication in phan- eroterid bushcrickets: Species-specific delay of female stridulatory re- sponse and matching male sensory time window. Behavioral Ecology and Sociobiology 18: 189-198. https://doi.org/10.1007/BF00290822 Heller K-G, von Helversen D (1993) Calling behavior in bushcrickets of the genus Poecilimon with differing communication systems (Orthop- tera: Tettigonioidea, Phaneropteridae). Journal of Insect Behavior 6: 361-377. https://doi.org/10.1007/BF01048117 Heller K-G, von Helversen O, Sergejeva M (1997b) Indiscriminate re- sponse behaviour in a female bushcricket: Sex role reversal in selectiv- ity of acoustic mate recognition? Naturwissenschaften 84: 252-255. https://doi.org/10.1007/s001140050391 von Helversen D, von Helversen O, Heller K-G (2012) When to give up re- sponding acoustically in Poecilimon bushcrickets: a clue to population density. Articulata 27: 57-66. von Helversen O, von Helversen D, Rohrseitz K, Koopmann I, Stumpner A, Heller K-G (2015) Signals and sex-specific active space in a duetting insect (Orthoptera: Phaneropteridae: Poecilimon affinis). Journal of Or- thoptera Research 24: 19-28. https://doi.org/10.1665/034.024.0104 Hennig RM, Franz A, Stumpner A (2004) Processing of auditory informa- tion in insects. Microscopy Research and Technique 63: 351-374. https://doi.org/10.1002/jemt.20052 Hildebrandt KJ (2014) Neural maps in insect versus vertebrate auditory systems. Current Opinion in Neurobiology 24: 82-87. https://doi. org/10.1016/j.conb.2013.08.020 H6bel G, Schul J (2007) Listening for males and bats: Spectral process- ing in the hearing organ of Neoconocephalus bivocatus (Orthoptera: Tettigoniidae). Journal of Comparative Physiology A 193: 917-925. https://doi.org/10.1007/s00359-007-0245-7 Hoy RR (1992) The evolution of hearing in insects as adaptation to preda- tion from bats. In: Webster DB, Fay RR, AN Popper (Eds) The Evolu- tionary Biology of Hearing. Springer, Heidelberg, 115-129. https:// doi.org/10.1007/978-1-4612-2784-7_8 Hoy RR (1998) Acute as a bug’s ear: An informal discussion of hearing in insects. In: Hoy RR, Popper AN, Fay RR (Eds) Comparative Hear- ing: Insects. Springer, New York, 1-17. https://doi.org/10.1007/978- 1-4612-0585-2_1 J. STRAUS Hoy RR, Robert D (1996) Tympanal hearing in insects. Annual Review of Entomology 41: 433-445. https://doi.org/10.1146/annurev. en.41.010196.002245 Hummel J, Koss] M, Nowotny M (2011) Sound-induced tympanal mem- brane motion in bushcrickets and its relationship to sensory out- put. Journal of Experimental Biology 214: 3596-3692. https://doi. org/10.1242/jeb.054445 Hummel J, Késsl M, Nowotny M (2017) Morphological basis for a tono- topic design of an insect ear. The Journal of Comparative Neurology 525: 2443-2455. https://doi.org/10.1002/cne.24218 Ingrisch I, Rentz DCF (2009) Orthoptera (Grasshoppers, Locusts, Katydids, Crickets). In Resh VH, Cardé RT (Eds) Encyclopedia of Insects (2"4 edn). Academic Press, Amsterdam, 732-743. https://doi.org/10.1016/ B978-0-12-374144-8.00196-X Jones PL, Page RA, Ratcliffe JM (2014) To scream or to listen? Prey detec- tion and discrimination in animal-eating bats. In: Fenton MB, Grin- nell AD, Popper AN, Fay RR (Eds) Bat Bioacoustics. Springer, Berlin, 93-116. https://doi.org/10.1007/978-1-4939-3527-7_4 Jonsson T, Montealegre-Z FE, Soulsbury CD, Robson Brown KA, Robert D (2016) Auditory mechanics in a bush-cricket: Direct evidence of dual sound inputs in the pressure difference receiver. Journal of the Royal Society Interface 13: 20160560. https://doi.org/10.1098/ rsif.2016.0560 Kalka M, Smith AR, Kalko EKV (2008) Bats limit arthropods and her- bivory in a tropical forest. Science 320: 71. https://doi.org/10.1126/ science. 1153352 Kalmring K, Ebendt R, Ahi J, Hellweg J, Young D, Halex H, Lakes R, Rossler W, Schréder J (1990) Comparative investigation on the morphology and physiology of the auditory receptor organs of seven species of bushcrickets. In: Gribakin FG, Wiese K, Popov AV (Eds) Sensory Systems and Communication in Arthropods. Birkhauser, Basel, 241-247. https://doi.org/10.1007/978-3-0348- 6410-7_41 Kalmring K, Hoffmann E, Jatho M, Sickmann T, Grossbach M (1996) The auditory-vibratory sensory system of the bushcricket Polysarcus denticauda (Phaneropterinae, Tettigoniidae). I]. Physiology of recep- tor cells. Journal of Experimental Zoology 276: 315-332. https:// doi.org/10.1002/(SICI)1097-010X(19961201)276:5%3C315::AID- JEZ2%3E3.0.CO;2-R Kalmring K, Rossler W, Ahi J, Ebendt R, Lakes R (1993) The auditory re- ceptor organs in the forelegs of tettigoniids. Physiology, receptor cell arrangement and morphology of the organs in Psorodonotus illyricus, Decticus albifrons and Decticus verrucivorus, (Orthoptera, Tettigonii- dae). Mitteilungen der Deutschen Gesellschaft fiir Allgemeine und Angewandte Entomologie 8: 663-668. Kalmring K, Réssler W, Ebendt R, Ahi J, Lakes R (1992) Structure, recep- tor cell arrangement and function of the auditory organs in the fore- leg tibia of three bushcricket species. Acta Biologica Hungarica 43: 441-449, Kalmring K, Rossler W, Hoffmann E, Jatho M, Unrast C (1995b) Causes of the differences in detection of low frequencies in the auditory re- ceptor organs of two species of bushcrickets. Journal of Experimental Zoology 272: 103-115. https://doi.org/10.1002/jez.1402720204 Kalmring K, Réssler W, Jatho M, Hoffmann E (1995a) Comparison of song frequency and receptor tuning in two closely related bushcricket spe- cies. Acta Biologica Hungaria 46: 457-469. Kalmring K, Réssler W, Unrast C (1994) Complex tibial organs in the forelegs, midlegs, and hindlegs of the bushcricket Gampsocleis gratiosa (Tettigoniidae): Comparison of the physiology of the organs. Jour- nal of Experimental Zoology 270: 155-161. https://doi.org/10.1002/ jez.1402700205 Kilmer MK, Barrus BB, Schul J (2010) Ultrasound avoidance behaviors in two species of Neoconocephalus (Orthoptera, Tettigoniidae). Journal of Orthoptera Research 19: 81-88. https://doi.org/10.1665/034.019.0114 Klose M (1996) Development of leg chordotonal sensory organs in nor- mal and heat shocked embryos of the cricket Teleogryllus commodus (Walker). Roux’s Archives of Developmental Biology 205: 344-355. https://doi.org/10.1007/BF00377214 JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS Knetsch H (1939) Die Korrelation der Ausbildung der Tympanalorgane, der Fliigel, der Stridulationsapparate und anderer Organsysteme bei den Orthopteren. Archiv fiir Naturgeschichte 8: 1-69. Kowalski K (2010) Vergleichende Untersuchungen zum akustischen Kom- munikationssystem der Tettigoniiden mit besonderer Beriicksichti- gung der Hetrodinae. PhD thesis, GiefSen, Germany: Justus-Liebig- Universitat Giefsen. Kowalski K, Lakes-Harlan R (2013) The acoustic communication system in six species of armoured ground crickets (Orthoptera: Tettigonii- dae: Hetrodinae): Commonalities and species-specific differences. Zoologischer Anzeiger 252: 204-216. https://doi.org/10.1016/j. jcz.2012.05.005 Lakes R, Schikorski T (1990) Neuroanatomy of Tettigoniids. In: Bailey WJ, Rentz DCF (Eds) The Tettigoniidae: Biology, Systematics and Evolution. Crawford House Press, Bathurst, 166-190. https://doi. org/10.1007/978-3-662-02592-5_10 Lakes-Harlan R, Bailey WJ, Schikorski T (1991) The auditory system of an atympanate bushcricket Phasmodes ranatriformes (Westwood) (Tettigo- niidae: Orthoptera). Journal of Experimental Biology 158: 307-324. Lakes-Harlan R, Scherberich J (2015) Position-dependent hearing in three species of bushcrickets (Tettigoniidae, Orthoptera). Royal Society Open Science 2: 140473. https://doi.org/10.1098/rsos.140473 Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The meta- bolic cost of neural information. Nature Neuroscience 1: 36-41. htt- ps://doi.org/10.1038/236 Lehmann AW (1998) Artbildung, akustische Kommunikation und sex- uelle Selektion bei griechischen Laubheuschrecken der Poecilimon pro- pinquus-Gruppe. PhD Thesis. Erlangen-Niirnberg, Germany Friedrich- Alexander-Universitat. Lehmann GUC, Siozios S, Bourtzis K, Reinhold K, Lehmann AW (2011) Thelytokous parthenogenesis and the heterogeneous decay of mat- ing behaviours in a bushcricket (Orthopteroida). Journal of Zoologi- cal Systematics and Evolutionary Research 49: 102-109. https://doi. org/10.1111/j.1439-0469.2010.00588.x Lehmann GUC, Strauf J, Lakes-Harlan R (2007) Listening when there is no sexual signalling? Maintenance of hearing in the asexual bush- cricket Poecilimon intermedius. Journal of Comparative Physiology A 193: 537-545. https://doi.org/10.1007/s00359-007-0209-y Lewis DB (1974) The physiology of the Tettigoniid ear. I. The implications of the anatomy of the ear to its function in sound reception. Journal of Experimental Biology 60: 821-837. http://jeb.biologists.org/con- tent/60/3/821.long Libersat F Hoy RR (1991) Ultrasonic startle behavior in bushcrickets (Or- thoptera; Tettigoniidae). Journal of Comparative Physiology A 169: 507-514. https://doi.org/10.1007/BF00197663 Lin Y, Réssler W, Kalmring K (1994) Complex tibial organs in fore-, mid-, and hindlegs of the bushcricket Gampsocleis gratiosa (Tettigoniidae): Comparison of morphology of the organs. Journal of Morphology 221: 191-198. https://doi.org/10.1002/jmor. 1052210208 Mason AC (1991) Hearing in a primitive ensiferan: the auditory system of Cyphoderris monstrosa (Orthoptera: Haglidae). Journal of Comparative Physiology A 168:351-363. https://doi.org/10.1007/BF00198354 Mason AC, Bailey WJ (1998) Ultrasound hearing and male-male commu- nication in Australian katydids (Tettigoniidae: Zaprochilinae) with sexually dimorphic ears. Physiological Entomology 23: 139-149. https://doi.org/10.1046/j.1365-3032.1998.232069.x Mason AC, Morris G, Wall P (1991) High ultrasonic hearing and tympa- nal slit function in rainforest katydids. Naturwissenschaften 78: 365- 367. https://doi.org/10.1007/BF01131611 Meier T, Reichert H (1990) Embryonic development and evolutionary ori- gin of the orthopteran auditory organs. Journal of Neurobiology 21: 592-610. https://doi.org/10.1002/neu.480210407 Michel K (1974) Das Tympanalorgan von Gryllus bimaculatus Degeer (Sal- tatoria, Gryllidae). Zeitschrift fiir Morphologie der Tiere 77: 285-315. https://doi.org/10.1007/BF00298805 Michel K (1979) Ein neuer Typ eines Grillenohres: Konstruktion und UI- trastruktur des Tympanalorgans von Cycloptiloides canariensis (Bolivar) (Mogoplistinae, Gryllidae). Zoologischer Anzeiger 203: 139-150. 217 Michel K, Petersen M (1982) Development of the tympanal organ in larvae of the migratory locust (Locusta migratoria). Cell and Tissue Research 222: 667-676. https://doi.org/10.1007/BF00213864 Michelsen A, Heller K-G, Stumpner A, Rohrseitz K (1994) A new biophysi- cal method to determine the gain of the acoustic trachea in bushcrick- ets. Journal of Comparative Physiology A 175: 145-151. https://doi. org/10.1007/BF00215110 Montealegre-Z F Jonsson T, Robson-Brown KA, Postles M, Robert D (2012) Convergent evolution between insect and mammalian audition. Sci- ence 338: 968-971. https://doi.org/10.1126/science.1225271 Montealegre-Z F, Morris GK, Mason AC (2006) Generation of extreme ul- trasonics in rainforest katydids. Journal of Experimental Biology 209: 4923-4937. https://doi.org/10.1242/jeb.02608 Montealegre-Z E Robert D (2015) Biomechanics of hearing in katy- dids. Journal of Comparative Physiology A 201: 5-18. https://doi. org/10.1007/s00359-014-0976-1 Morris GK, Mason AC, Wall P, Belwood JJ (1994) High ultrasonic and tremulation signals in neotropical katydids (Orthoptera: Tettigoniidae). Journal of Zoology 233: 129-163. https://doi. org/10.1111/j.1469-7998.1994.tb05266.x Mugleston JD, Song H, Whiting MF (2013) A century of paraphyly: A mo- lecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like wings. Molecular Phylogenetics and Evo- lution 69: 1120-1134. https://doi.org/10.1016/j.ympev.2013.07.014 Nickle DA (2006) Two new arboreal species of pseudophylline katy- dids from northern Peru (Orthoptera: Tettigoniidae: Pseudophyl- linae). Journal of Orthoptera Research 15: 31-36. https://doi. org/10.1665/1082-6467(2006) 15[31:TNASOP]2.0.CO;2 Nickle DA, Carlysle TC (1975) Morphology and function of female sound- producing structures in ensiferan Orthoptera with special emphasis on the Phaneropterinae. International Journal of Insect Morphol- ogy and Embryology 4: 159-168. https://doi.org/10.1016/0020- 7322(75)90014-8 Nocke H (1975) Physical and physiological properties of the tettigoniid (“Grasshopper”) ear. Journal of Comparative Physiology 100: 25-57. https://doi.org/10.1007/BF00623929 Oldfield BP (1982) Tonotopic organisation of auditory receptors in Tet- tigoniidae (Orthoptera: Ensifera). Journal of Comparative Physiology 147: 461-469. https://doi.org/10.1007/BF00612011 Oldfield BP (1984) Physiology of auditory receptors in two species of Tetti- goniidae (Orthoptera: Ensifera). Alternative tonotopic organisations of the auditory organ. Journal of Comparative Physiology A 155: 689-696. https://doi.org/10.1007/BF00610855 Oldfield BP (1985) The tuning of auditory receptors in bushcrickets. Hearing Research 17: 21-35. https://doi.org/10.1016/0378-5955(85)90126-1 Ostrowski TD, Stumpner A (2010) Frequency processing at consecutive lev- els in the auditory system of bush crickets (Tettigoniidae). The Journal of Comparative Neurology 518: 3101-3116. https://doi.org/10.1002/ cne.22385 Palghat Udayashankar A, Késsl M, Nowotny M (2012) Tonotopically ar- ranged traveling waves in the miniature hearing organ of bushcrickets. PLoS ONE 7: e310008. https://doi.org/10.1371/journal.pone.0031008 Pollack GS (1998) Neural processing of acoustic signals. In: Hoy RR, Pop- per AN, Fay RR (Eds) Comparative Hearing: Insects. Springer, New York, 139-196. https://doi.org/10.1007/978-1-4612-0585-2_5 Pollack GS (2015) Neurobiology of acoustically mediated predator detec- tion. Journal of Comparative Physiology A 201: 99-109. https://doi. org/10.1007/s00359-014-0948-5 Pollack GS, Hedwig B (2017) The cricket auditory pathway: Neural process- ing of acoustic signals. In: Horch HW, Mito T, Popadié A, Ohuchi H, Noji S (Eds) The Cricket as Model Organism. Development, Regener- ation and Behavior. Springer, 155- 167. https://doi.org/10.1007/978- 4-431-56478-2_11 Rajaraman K, Mhatre N, Jain M, Postles M, Balakrishnan R, Robert D (2013) Low-pass filters and differential tympanal tuning in a paleo- tropical bushcricket with an unusually low frequency call. Journal of Experimental Biology 216: 777-787. https://doi.org/10.1242/ jeb.078352 JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) 218 Rentz DCF (1993) Tettigoniidae of Australia Volume 2: Austrosaginae, Zaprochilinae and Phasmodinae. CSIRO Publishing, Victoria, 386 pp. https://doi.org/10.1071/9780643105317 Rentz DCF (2001) Tettigoniidae of Australia Volume 3: The Listros- celidinae, Tympanophorinae, Meconematinae and _ Miéicrotetti- goniinae. CSIRO Publishing, Collingwood, 524 pp. https://doi. org/10.1071/9780643105324 Robinson DJ, Hall MJ (2002) Sound signalling in Orthoptera. Advances in Insect Physiology 29: 151-278. https://doi.org/10.1016/S0065- 2806(02)29003-7 Romer H (1983) Tonotopic organization of the auditory neuropile in the bushcricket Tettigonia viridissima. Nature 306: 60-62. https://doi. org/10.1038/306060a0 Romer H (2016) Matched filters in insect audition: Tuning curves and beyond. In: von der Emde G, Warrant E (Eds) The Ecology of Ani- mal Senses. Matched Filters for Economical Sensing. Springer, Cham, 83-109. https://doi.org/10.1007/978-3-319-25492-0_4 Romer H (2018) Acoustic communication. In: Cdérdoba-Aguilar A, Gonzalez-Tokman D, Gonzalez-Santoyo I (Eds) Insect Behavior: From Mechanisms to Ecological and Evolutionary Consequences. Oxford University Press, Oxford, 174-188. https://doi.org/10.1093/ o0so/9780198797500.003.0012 Romer H, Bailey WJ (1998) Strategies for hearing in noise: Peripheral control over auditory-sensitivity in the bushcricket Sciarasaga quad- rata (Australosaginae, Tettigoniidae). Journal of Experimental Biol- ogy 201: 1023-1033. http://jeb.biologists.org/content/201/7/1023. long Romer H, Lang A, Hartbauer M (2008) No correlation of body size and high-frequency hearing sensitivity in neotropical phaneropterine katydids. Journal of Orthoptera Research 17: 343-346. https://doi. org/10.1665/1082-6467-17.2.343 Romer H, Lewald J (1992) High-frequency sound transmission in natural habitats: Implications for the evolution of insect acoustic communi- cation. Behavioral Ecology and Sociobiology 29: 437-444. https:// doi.org/10.1007/BF00170174 Romer H, Spickermann M, Bailey W (1998) Sensory basis for sound inten- sity discrimination in the bushcricket Requena verticalis (Tettigoniidae, Orthoptera). Journal of Comparative Physiology A 182: 595-607. https://doi.org/10.1007/s003590050206 Roéssler W (1992a) Postembryonic development of the complex tibial or- gan in the foreleg of the bushcricket Ephippiger ephippiger (Orthoptera, Tettigoniidae). Cell and Tissue Research 269: 505-514. https://doi. org/10.1007/BF00353905 Réssler W (1992b) Functional morphology and development of tibial organs in the legs I, II and III of the bushcricket Ephippiger ephippi- ger (Insecta, Ensifera). Zoomorphology 112: 181-188. https://doi. org/10.1007/BF01633108 Roéssler W, Bailey WJ, Schréder J, Kalmring K (1990) Resolution of time and frequency patterns in the tympanal organs of Tettigoniids I. Syn- chronization and oscillation in the activity of receptor populations. Zoologische Jahrbiicher, Abteilung ftir allgemeine Zoologie und Physiologie der Tiere 94: 83-99. Réssler W, Hiibschen A, Schul J, Kalmring K (1994) Functional morphol- ogy of bushcricket ears: Comparison between two species belonging to the Phaneropterinae and Decticinae (Insecta, Ensifera). Zoomor- phology 114: 39-46. https://doi.org/10.1007/BF00574913 Rossler W, Jatho M, Kalmring K (2006) The auditory-vibratory sensory sys- tem in bushcrickets (Tettigoniidae, Ensifera, Orthoptera. In: Droso- poulos S, Claridge M, editors. Insect Sounds and Communication: Physiology, Behaviour, Ecology and Evolution. CRC Press, Boca Ra- ton, 35-69. https://doi.org/10.1201/9781420039337.ch3 Roéssler W, Kalmring K (1994) Similar structural dimensions in bushcrick- et auditory organs in spite of different foreleg size: Consequences for auditory tuning. Hearing Research 80: 191-196. https://doi. org/10.1016/0378-5955(94)90110-4 J. STRAUS Sarria-S FA, Chivers DB, Soulsbury CD, Montealegre-Z F (2017) Non-invasive biophysical measurements of travelling waves in the insect inner ear. Roy- al Society Open Science 4: 170171. https://doi.org/10.1098/rsos.170171 Sarria-S FA, Morris GK, Windmill JFC, Jackson J, Montealegre-Z F (2014) Shrinking wings for ultrasonic pitch production: Hyperintense ultra-short-wavelength calls in a new genus of neotropical katy- dids (Orthoptera: Tettigoniidae). PLoS ONE 9: e98708. https://doi. org/10.1371/journal.pone.0098708 Scherberich J, Hummel J, Sch6neich S, Nowotny M (2016) Auditory fo- vea in the ear of a duetting katydid shows male-specific adaptations to the female call. Current Biology 26: R1222-R1223. https://doi. org/10.1016/j.cub.2016.10.035 Scherberich J, Hummel J, Schéneich S, Nowotny M (2017) Functional basis of the sexual dimorphism in the auditory fovea of the duet- ting bushcricket Ancylecha fenestrata. Proceedings of the Royal Soci- ety B: Biological Sciences 284: 20171426. https://doi.org/10.1098/ rspb.2017.1426 Schneider ES, Romer H, Robillard T, Schmidt AKD (2017) Hearing with ex- ceptionally thin tympana: Ear morphology and tympanal membrane vibrations in eneopterine crickets. Scientific Reports 7: 15266. https:// doi.org/10.1038/s41598-017-15282-z Schul J, Bush SL, Frederick KH (2014) Evolution of call patterns and pat- tern recognition mechanisms in Neoconocephalus katydids. In: Hed- wig B (Ed.) Insect Hearing and Acoustic Communication. Springer, New York, 167-183. https://doi.org/10.1007/978-3-642-40462-7_10 Schul J, Patterson AC (2003) What determines the tuning of hearing organs and the frequency of calls? A comparative study in the ka- tydid genus Neoconocephalus (Orthoptera, Tettigoniidae). Journal of Experimental Biology 206: 141-152. https://doi.org/10.1242/ jeb.00070 Schul J, Rdossler W (1993) Processing of complex song parameters by paral- lel neuronal activity within the auditory system of two closely related bushcricket species. Zoologische Jahrbiicher, Abteilung fir allge- meine Zoologie und Physiologie der Tiere 97: 95-110. Schulze W, Schul J (2001) Ultrasound avoidance behaviour in the bush- cricket Tettigonia viridissima (Orthoptera: Tettigoniidae). Journal of Experimental Biology 204: 733-740. http://jeb.biologists.org/con- tent/204/4/733.long Schumacher R (1973) Morphologische Untersuchungen der tibialen Tym- panalorgane von neun einheimischen Laubheuschrecken-Arten (Or- thoptera, Tettigonioidea). Zeitschrift fiir Morphologie der Tiere 75: 267-282. https://doi.org/10.1007/BF00288474 Schumacher R (1975a) Scanning-electron-microscope description of the tibial tympanal organ of the Tettigonioidea (Orthoptera, Ensif- era). Zeitschrift fiir Morphologie der Tiere 81: 209-219. https://doi. org/10.1007/BF00278370 Schumacher R (1975b) Vergleich des primaren Rezeptorbereichs der tympanalen und atympanalen tibialen Skolopalorgane von 14 mit- teleuropadischen Laubheuschrecken-Arten (Orthoptera: Tettigo- nioidea). Entomologia Germanica 1: 97-104. Schumacher R (1979) Zur funktionellen Morphologie des auditorischen Systems der Laubheuschrecken. Entomologia Generalis 5: 321-356. Schwabe J (1906) Beitrage zur Morphologie und Histologie der tympana- len Sinnesapparate der Orthopteren. Zoologica 50: 1-154. Sickmann T, Kalmring K, Miller A (1997) The auditory-vibratory system of the bushcricket Polysarcus denticauda (Phaneropterinae, Tettigoniidae) I. Morphology of the complex tibial organs. Hearing Research 104: 155-166. https://doi.org/10.1016/S0378-5955(96)00194-3 Sismondo E (1980) Physical characteristics of the drumming of Meconema thalassinum. Journal of Insect Physiology 26: 209-212. https://doi. org/10.1016/0022-1910(80)90082-7 Stied] O, Kalmring K (1989) The importance of song and vibratory signals in the behaviour of the bushcricket Ephippiger ephippiger Fiebig (Or- thoptera, Tettigoniidae): Taxis by females. Oecologia 80: 142-144. https://doi.org/10.1007/BF00789945 JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2) J. STRAUS Stdélting H, Stumpner A (1998) Tonotopic organization of auditory recep- tor cells in the bushcricket Pholidoptera griseoaptera (Tettigoniidae, Decticinae). Cell and Tissue Research 294: 377-386. https://doi. org/10.1007/s004410051187 Straufg J, Alt JA, Ekschmitt K, Schul J, Lakes-Harlan R (2017) Evolution- ary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life hisstory. Jour- nal of Evolutionary Biology 30: 1094-1109. https://doi.org/10.1111/ jeb.13066 Straus J, Lakes-Harlan R (2008) Neuroanatomy of the complex tibial organ of Stenopelmatus (Orthoptera: Ensifera: Stenopelmatidae). The Jour- nal of Comparative Neurology 511: 81-91. https://doi.org/10.1002/ cne.21836 Straufs J, Lakes-Harlan R (2010) Neuroanatomy of the complex tibial organ in the splay-footed cricket Comicus calcaris Irish 1986 (Orthoptera: Ensifera: Schizodactylidae). The Journal of Comparative Neurology 518: 4567-4580. https://doi.org/10.1002/cne.22478 Straus J, Lehmann AW, Lehmann GUC (2014) Sensory evolution of hear- ing in tettigoniids with differing communication systems. Journal of Evolutionary Biology 27: 200-213. https://doi.org/10.1111/jeb.12294 Strauf§ J, Lehmann GUC, Lehmann AW, Lakes-Harlan R (2012) Spatial organization of tettigoniid auditory receptors: Insights from neu- ronal tracing. Journal of Morphology 273: 1280-1290. https://doi. org/10.1002/jmor.20058 Strauf§ J, Riesterer AS, Lakes-Harlan R (2016) How many mechanosen- sory organs in the bushcricket leg? Neuroanatomy of the scolopidial accessory organ in Tettigoniidae (Insecta: Orthoptera). Arthropod Structure and Development 45: 31-41. https://doi.org/10.1016/j. asd.2015.11.002 Strauf J, Stumpner A (2015) Selective forces on origin, adaptation and reduction of tympanal ears in insects. Journal of Comparative Physi- ology A 201: 155-169. https://doi.org/10.1007/s00359-014-0962-7 Stumpner A (1996) Tonotopic organization of the hearing organ in a bushcricket. Physiological characterization and complete staining of auditory receptor cells. Naturwissenschaften 83: 81-84. https://doi. org/10.1007/BF01141875 Stumpner A, Heller K-G (1992) Morphological and physiological differ- ences of the auditory system in three related bushcrickets (Orthop- tera: Phaneropteridae, Poecilimon). Physiological Entomology 17: 73-80. https://doi.org/10.1111/j.1365-3032.1992.tb00992.x 219 Stumpner A, von Helversen D (2001) Evolution and function of auditory systems in insects. Naturwissenschaften 88: 159-170. https://doi. org/10.1007/s001140100223 Stumpner A, Nowotny M (2014) Neural processing in the bush-cricket au- ditory pathway. In Hedwig B (Ed.) Insect Hearing and Acoustic Com- munication. Springer, Berlin, 143-166. https://doi.org/10.1007/978- 3-642-40462-7_9 ter Hofstede HM, Kalko EKV, Fullard JH (2010) Auditory-based defence against gleaning bats in neotropical katydids (Orthoptera: Tettigo- niidae). Journal of Comparative Physiology A 196: 349-358. https:// doi.org/10.1007/s00359-010-0518-4 ter Hofstede H, Voigt-Heucke S, Lang A, ROmer H, Page R, Faure P, Dechmann D (2017) Revisiting adaptations of neotropical katydids (Orthoptera: Tettigoniidae) to gleaning bat predation. Neotropical Biodiversity 3: 41-49. https://doi.org/10.1080/23766808.2016.12 72314 Vahed K (1996) Prolonged copulation in oak bushcrickets (Tettigoniidae: Meconematinae: Meconema thalassinum and M. meridionale). Journal of Orthoptera Research 5: 199-204. https://doi.org/10.2307/3503594 Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Micrscopy Research and Technique 63: 315-337. https:// doi.org/10.1002/jemt.20051 Yack JE, Dawson JW (2007) Insect ears. In: Basbaum AI, Kaneko A, Shep- herd GM, Westheimer G (Eds) The Senses: A Comprehensive Refer- ence, Vol 3 Audition. Academic Press, San Diego, 35-54. https://doi. org/10.1016/B978-012370880-9.00003-7 Yager DD (1999) Structure, development, and evolution of insect auditory systems. Microscopy Research and Technique 47: 380-400. https:// doi.org/10.1002/(SICI)1097-0029(19991215)47:6%3C380::AID- JEMT3%3E3.0.CO;2-P Zhantiev RD, Korsunovskaya OS (1978) Morphofunctional organization of tympanal organs in Tettigonia cantans (Orthoptera, Tettigoniidae). Zoologiceskij Zurnal 57: 1012-1016. Zhantiev RD, Korsunovskaya OS, Bysov SD (1995) Acoustic communica- tion in desert bush-crickets (Orthoptera, Bradyporidae). Zoologiceskij Zurnal 74: 58-72. JOURNAL OF ORTHOPTERA RESEARCH 2019, 28(2)