Johannes Strauß

Listening when there is no sexual signalling? Maintenance of hearing in the asexual bushcricket Poecilimon intermedius.

Unisexual reproduction is a widespread phenomenon in invertebrates and lower vertebrates. If a former sexual reproducing species becomes parthenogenetic, we expect traits that were subject to sexual selection to diminish. The bushcricket Poecilimon intermedius is one of the few insect species with obligate but diploid parthenogenetic reproduction. We contrasted characters that are involved in mating in a sexually sibling species with the identical structures in the parthenogenetic P. intermedius. Central for sexual communication are male songs, while receptive females approach the males phonotactically. Compared to its sister-species P. ampliatus, the morphology of the hearing organs (acoustic spiracle, crista acustica) and the function of hearing (acoustic threshold) are reduced in P. intermedius. Nonetheless, hearing is clearly maintained in the parthenogenetic females. Natural selection by acoustic hunting bats, pleiotropy or a developmental trap may explain the well maintained hearing function.

Neuroanatomy of the Complex Tibial Organ of Stenopelmatus (Orthoptera: Ensifera: Stenopelmatidae)

Stenopelmatidae (or “Jerusalem crickets”) belong to the atympanate Ensifera, lacking hearing organs in the foreleg tibiae. Their phylogenetic position is controversial, either as a taxon in Tettigonioidea or within the clade of Gryllacridoidea. Similarly, the origin of tibial auditory systems in Ensifera is controversial. Therefore, we investigated the neuronal structures of the proximal tibiae of Stenopelmatus spec. with the hypothesis that internal sensory structures are similar to those in tympanate Ensifera. In Stenopelmatus the complex tibial organ consists of three neuronal parts: the subgenual organ, the intermediate organ, and a third part with linearly arranged neurons. This tripartite organization is also found in tympanate Ensifera, verifying our hypothesis. The third part of the sense organ found in Stenopelmatus can be regarded by the criterion of position as homologous to auditory receptors of hearing Tettigonioidea. This crista acustica homolog is found serially in all thoracic leg pairs and contains 20 ± 2 chordotonal neurons in the foreleg. The tibial organ was shown to be responsive to vibration, with a broad threshold of about 0.06 ms−2 in a frequency range from 100–600 Hz. The central projection of tibial sensory neurons terminates into two equally sized lobes in the primary sensory neuropil, the medial ventral association center. The data are discussed comparatively to those of other Ensifera and mapped phylogenetically onto recently proposed phylogenies for Ensifera. The crista acustica homolog could represent a neuronal rudiment of a secondarily reduced ear, but neuronal features are also consistent with an evolutionary preadaptation. J. Comp. Neurol. 511:81–91, 2008.

The evolutionary origin of auditory receptors in Tettigonioidea: the complex tibial organ of Schizodactylidae

Audition in insects is of polyphyletic origin. Tympanal ears derived from proprioceptive or vibratory receptor organs, but many questions of the evolution of insect auditory systems are still open. Despite the rather typical bauplan of the insect body, e.g., with a fixed number of segments, tympanal ears evolved at very different places, but only ensiferans have ears at the foreleg tibia, located in the tibial organ. The homology and monophyly of ensiferan ears is controversial, and no precursor organ was unambiguously identified for auditory receptors. The latter can only be identified by comparative study of recent atympanate taxa. These atympanate taxa are poorly investigated. In this paper, we report the neuroanatomy of the tibial organ of Comicus calcaris (Irish 1986), an atympanate Schizodactylid (splay-footed cricket). This representative of a Gondwana relict group has a tripartite sensory organ, homologous to tettigoniid ears. A comparison with morphology-based cladistic phylogeny indicates that the tripartite neuronal organization present in the majority of Tettigonioidea presumably preceded evolution of a hearing sense in the Tettigonioidea. Furthermore, the absence of a tripartite organ in Grylloidea argues against a monophyletic origin and homology of the cricket and katydid ears. The tracheal attachment of sensory neurons typical for ears of Tettigonioidea is present in C. calcaris and may have facilitated cooption for auditory function. The functional auditory organ was presumably formed in evolution by successive non-neural modifications of trachea and tympana. This first investigation of the neuroanatomy of Schizodactylidae suggests a non-auditory chordotonal organ as the precursor for auditory receptors of related tympanate taxa and adds evidence for the phylogenetic position of the group.

Spatial organization of tettigoniid auditory receptors: Insights from neuronal tracing

The auditory sense organ of Tettigoniidae (Insecta, Orthoptera) is located in the foreleg tibia and consists of scolopidial sensilla which form a row termed crista acustica. The crista acustica is associated with the tympana and the auditory trachea. This ear is a highly ordered, tonotopic sensory system. As the neuroanatomy of the crista acustica has been documented for several species, the most distal somata and dendrites of receptor neurons have occasionally been described as forming an alternating or double row. We investigate the spatial arrangement of receptor cell bodies and dendrites by retrograde tracing with cobalt chloride solution. In six tettigoniid species studied, distal receptor neurons are consistently arranged in double‐rows of somata rather than a linear sequence. This arrangement of neurons is shown to affect 30–50% of the overall auditory receptors. No strict correlation of somata positions between the anterio‐posterior and dorso‐ventral axis was evident within the distal crista acustica. Dendrites of distal receptors occasionally also occur in a double row or are even massed without clear order. Thus, a substantial part of auditory receptors can deviate from a strictly straight organization into a more complex morphology. The linear organization of dendrites is not a morphological criterion that allows hearing organs to be distinguished from nonhearing sense organs serially homologous to ears in all species. Both the crowded arrangement of receptor somata and dendrites may result from functional constraints relating to frequency discrimination, or from developmental constraints of auditory morphogenesis in postembryonic development. J. Morphol.

Selective forces on origin, adaptation and reduction of tympanal ears in insects

Insect ears evolved many times independently. As a consequence, a striking diversity exists in the location, construction and behavioural implementation of ears. In this review, we first summarise what is known about the evolutionary origin of ears and the presumed precursor organs in the various insect groups. Thereafter, we focus on selective forces for making and keeping an ear: we discuss detecting and localising predators and conspecifics, including establishing new “private” channels for intraspecific communication. More advanced aspects involve judging the distance of conspecifics, or assessing individual quality from songs which makes auditory processing a means for exerting sexual selection on mating partners. We try to identify negative selective forces, mainly in the context of energy expenditure for developing and keeping an ear, but also in conjunction with acoustic communication, which incorporates risks like eavesdropping by predators and parasitoids. We then discuss balancing pressures, which might oppose optimising an ear for a specific task (when it serves different functions, for example). Subsequently, we describe various scenarios that might have led to a reduction or complete loss of ears in evolution. Finally, we describe cases of sex differences in ears and potential reasons for their appearance.

Evolutionary and Phylogenetic Origins of Tympanal Hearing Organs in Insects

Among insects, tympanal ears evolved at least 18 times, resulting in a diversity of auditory systems. Insects use their ears in different behavioural contexts, mainly intraspecific communication for mate attraction, predator avoidance, and parasitic host localisation. Analysing the evolution of insect ears aims at revealing the phyletic origins of auditory organs, the selection pressures leading to the evolution of ears, the physiological and behavioural adaptations of hearing, and the diversification of ears in specific groups or lineages. The origin of sensory organs from preadapted proprioceptive or vibroceptive organs has now been established for different ear types. In this review, we embed research on insect hearing in a phylogenetic framework to reconstruct the ancestral sensory situation in different taxa, and the series of morphological changes during the evolution of an ear. The importance of sensory and neuroanatomical data is discussed for either mapping onto a phylogeny or as characters for phylogenetic analysis.

Neuroanatomy of the complex tibial organ in the splay-footed cricket Comicus calcaris Irish 1986 (Orthoptera: Ensifera: Schizodactylidae).

The subgenual chordotonal organ complex in insects is modified in ensiferan taxa like Gryllidae and Tettigoniidae into hearing organs with specific sets of auditory receptors. Here, this sensory organ complex is documented in the nonhearing splay‐footed cricket Comicus calcaris. The tibial chordotonal organ consists of three parts: the subgenual organ, the intermediate organ, and the crista acustica homolog. The latter is an array of linearly organized neurons homologous to auditory receptors in the tibial hearing organs of Tettigoniidae. The tibial organ is structurally similar in all three leg pairs, with similar neuron numbers in the fore‐ and midleg, but lower numbers in the hindleg. The foreleg crista acustica homolog consists of 34 ± 4 neurons, the highest number in an atympanate Ensiferan. Additionally, an accessory chordotonal organ with 15 ± 5 neurons innervated by nerve 5B1 is present in the foreleg. The central projection of the tibial organreveals ipsilateral sensory terminals in the primary sensory neuropil, the medial ventral association center with terminations close to the midline. As determined from extracellular recordings, the entire tibial organ is vibrosensitive. The organization of the tibial organ is compared to other ensiferan auditory and nonauditory tibial organs. Spatial orientation of neurons in the crista acustica homolog is not reminiscent of auditory structures, and the neuroanatomy is discussed with respect to stridulation behavior and the evolutionary origin of hearing in Ensifera. J. Comp. Neurol. 518:4567–4580, 2010.

Sensory neuroanatomy of stick insects highlights the evolutionary diversity of the orthopteroid subgenual organ complex

The subgenual organ is a scolopidial sense organ located in the tibia of many insects. In this study the neuroanatomy of the subgenual organ complex of stick insects is clarified for two species, Carausius morosus and Siyploidea sipylus. Neuronal tracing shows a subgenual organ complex that consists of a subgenual organ and a distal organ. There are no differences in neuroanatomy between the three thoracic leg pairs, and the sensory structures are highly similar in both species. A comparison of the neuroanatomy with other orthopteroid insects highlights two features unique in Phasmatodea. The subgenual organ contains a set of densely arranged sensory neurons in the anterior‐ventral part of the organ, and a distal organ with 16–17 scolopidial sensilla in C. morosus and 20–22 scolopidial sensilla in S. sipylus. The somata of sensory neurons in the distal organ are organized in a linear array extending distally into the tibia, with only a few exceptions of closely associated neurons. The stick insect sense organs show a case of an elaborate scolopidial sense organ that evolved in addition to the subgenual organ. The neuroanatomy of stick insects is compared to that studied in other orthopteroid taxa (cockroaches, locusts, crickets, tettigoniids). The comparison of sensory structures indicates that elaborate scolopidial organs have evolved repeatedly among orthopteroids. The distal organ in stick insects has the highest number of sensory neurons known for distal organs so far. J. Comp. Neurol. 521:3791–3803, 2013.

Sensory evolution of hearing in tettigoniids with differing communication systems.

In Tettigoniidae (Orthoptera: Ensifera), hearing organs are essential in mate detection. Male tettigoniids usually produce calling songs by tegminal stridulation, whereas females approach the males phonotactically. This unidirectional communication system is the most common one among tettigoniids. In several tettigoniid lineages, females have evolved acoustic replies to the male calling song which constitutes a bidirectional communication system. The genus Poecilimon (Tettigoniidae: Phaneropterinae) is of special interest because the ancestral state of bidirectional communication, with calling males and responding females, has been reversed repeatedly to unidirectional communication. Acoustic communication is mediated by hearing organs that are adapted to the conspecific signals. Therefore, we analyse the auditory system in the Tettigoniidae genus Poecilimon for functional adaptations in three characteristics: (i) dimension of sound‐receiving structures (tympanum and acoustic spiracle), (ii) number of auditory sensilla and (iii) hearing sensitivity. Profound differences in the auditory system correlate with uni‐ or bidirectional communication. Among the sound‐receiving structures, the tympana scale with body size, whereas the acoustic spiracle, the major sound input structure, was drastically reduced in unidirectional communicating species. In the unidirectional P. ampliatus group, auditory sensilla are severely reduced in numbers, but not in the unidirectional P. propinquus group. Within the P. ampliatus group, the number of auditory sensilla is further reduced in P. intermedius which lost acoustic signalling due to parthenogenesis. The auditory sensitivity correlated with the size of the acoustic spiracle, as hearing sensitivity was better with larger spiracles, especially in the ultrasonic range. Our results show a significant reduction in auditory structures, shaped by the differing sex roles during mate detection.

The subgenual organ complex in the cave cricket Troglophilus neglectus (Orthoptera: Rhaphidophoridae): comparative innervation and sensory evolution.

Comparative studies of the organization of nervous systems and sensory organs can reveal their evolution and specific adaptations. In the forelegs of some Ensifera (including crickets and tettigoniids), tympanal hearing organs are located in close proximity to the mechanosensitive subgenual organ (SGO). In the present study, the SGO complex in the non-hearing cave cricket Troglophilus neglectus (Rhaphidophoridae) is investigated for the neuronal innervation pattern and for organs homologous to the hearing organs in related taxa. We analyse the innervation pattern of the sensory organs (SGO and intermediate organ (IO)) and its variability between individuals. In T. neglectus, the IO consists of two major groups of closely associated sensilla with different positions. While the distal-most sensilla superficially resemble tettigoniid auditory sensilla in location and orientation, the sensory innervation does not show these two groups to be distinct organs. Though variability in the number of sensory nerve branches occurs, usually either organ is supplied by a single nerve branch. Hence, no sensory elements clearly homologous to the auditory organ are evident. In contrast to other non-hearing Ensifera, the cave cricket sensory structures are relatively simple, consistent with a plesiomorphic organization resembling sensory innervation in grasshoppers and stick insects.