Leader preference in Neoconocephalus ensiger katydids: a female preference for a nonheritable male trait.

Female preferences for males producing their calls just ahead of their neighbours, leader preferences, are common in acoustically communicating insects and anurans. While these preferences have been well studied, their evolutionary origins remain unclear. We tested whether females gain a fitness benefit by mating with leading males in Neoconocephalus ensiger katydids. We mated leading and following males with random females and measured the number and quality of F1 , the number of F2 and the heritability of the preferred male trait. We found that females mating with leaders and followers did not differ in the number of F1 or F2 offspring. Females mating with leading males had offspring that were in better condition than those mating with following males suggesting a benefit in the form of higher quality offspring. We found no evidence that the male trait, the production of leading calls, was heritable. This suggests that there is no genetic correlate for the production of leading calls and that the fitness benefit gained by females must be a direct benefit, potentially mediated by seminal proteins. The presence of benefits indicates that leader preference is adaptive in N. ensiger, which may explain the evolutionary origin of leader preference; further tests are required to determine whether fitness benefits can explain the phylogenetic distribution of leader preference in Neoconocephalus. The absence of heritability will prevent leader preference from becoming coupled with or exaggerating the male trait and prevent females from gaining a 'sexy-sons' benefit, weakening the overall selection for leader preference.

Evolutionary diversification of the auditory organ sensilla in Neoconocephalus katydids (Orthoptera: Tettigoniidae) correlates with acoustic signal diversification over phylogenetic relatedness and life history.

Neoconocephalus Tettigoniidae are a model for the evolution of acoustic signals as male calls have diversified in temporal structure during the radiation of the genus. The call divergence and phylogeny in Neoconocephalus are established, but in tettigoniids in general, accompanying evolutionary changes in hearing organs are not studied. We investigated anatomical changes of the tympanal hearing organs during the evolutionary radiation and divergence of intraspecific acoustic signals. We compared the neuroanatomy of auditory sensilla (crista acustica) from nine Neoconocephalus species for the number of auditory sensilla and the crista acustica length. These parameters were correlated with differences in temporal call features, body size, life histories and different phylogenetic positions. By this, adaptive responses to shifting frequencies of male calls and changes in their temporal patterns can be evaluated against phylogenetic constraints and allometry. All species showed well-developed auditory sensilla, on average 32-35 between species. Crista acustica length and sensillum numbers correlated with body size, but not with phylogenetic position or life history. Statistically significant correlations existed also with specific call patterns: a higher number of auditory sensilla occurred in species with continuous calls or slow pulse rates, and a longer crista acustica occurred in species with double pulses or slow pulse rates. The auditory sensilla show significant differences between species despite their recent radiation, and morphological and ecological similarities. This indicates the responses to natural and sexual selection, including divergence of temporal and spectral signal properties. Phylogenetic constraints are unlikely to limit these changes of the auditory systems.

Sensory-encoding differences contribute to species-specific call recognition mechanisms.

Object recognition is a fundamental function of the auditory system, but the underlying mechanisms are not well understood. Acoustic communication in the Tettigoniid genus Neoconocephalus provides a useful system for studying these mechanisms. We examined the ascending interneuron pathway in three Neoconocephalus species with diverse calls and recognition mechanisms. This pathway processes spectral information and transmits call temporal patterns to the supraesophageal ganglion where the recognition circuits reside. For each species, we describe one local auditory interneuron (ON) and three with ascending projections (AN-1, AN-2, TN-1), which were physiologically and morphologically similar to those described in other Tettigoniids. TN-1 responded only to the beginning of call models. For AN-1, each call model pulse elicited a single action potential in N. robustus and N. bivocatus, whereas every other pulse elicited an action potential in N. triops. Individual pulses did not reliably evoke AN-2 responses in all three species. AN-1 responses were limited to frequencies<20 kHz. AN-1 tuning differed among the three species, reflecting their differences in the dominant frequency of the calls. AN-2 was broadly tuned, and responses increased with intensity in all three species. In behavioral experiments, N. robustus showed greater spectral selectivity than the other two species. Adding the second harmonic to the spectrum of call models suppressed phonotaxis in N. robustus, but not N. triops or N. bivocatus. Adding the second harmonic reduced AN-1 responses in N. robustus but not in the other two species. We discuss the potential function of the ascending neurons for call recognition.

Auditory stream segregation in an insect.

Auditory stream segregation is the perceptual grouping of the acoustic mixture reaching the ear into coherent representations of sound sources. It has been described in a variety of vertebrates and underlies auditory scene analysis or auditory image formation. Here we describe a phenomenon in an invertebrate that bears an intriguing resemblance to auditory stream segregation observed in vertebrates: in Neoconocephalus retusus (Orthoptera, Tettigoniidae) an auditory interneuron segregates information about bat echolocation calls from background male advertisement songs. This process utilizes differences between the temporal and spectral characteristics of the two stimuli, a mechanism which is similar to those of auditory stream segregation in vertebrates. This similarity suggests that auditory stream segregation is a fundamental feature of auditory perception, widespread from invertebrates to humans.

Phonotaxis during walking and flight: are differences in selectivity due to predation pressure?

Female selectivity was tested in Tettigonia viridissima during two different phonotaxis situations; compensated walking and tethered flight. For two of the three temporal parameters that are important for call recognition in T. viridissima, selectivity was similar in the two situations. Selectivity for the third parameter (minimum interval duration between the double pulses) was much higher during walking than during flight: walking females responded only to stimuli with intervals of 28 ms or longer, while call models with intervals of 18 ms were attractive during flight. One interneuron (TN-1) is probably involved in filtering the minimum interval duration. As this neuron is also the most likely candidate for transmitting bat calls during flight, it is suggested that the selectivity differences between walking and flying might be due to the need for detecting predator signals during flight, when TN-1 would be occupied listening for bats. With TN-1 unavailable for song processing during flight, temporal selectivity for the minimum interval duration should be reduced, as was found here.

Ultrasound avoidance behaviour in the bushcricket Tettigonia viridissima (Orthoptera: Tettigoniidae).

The responses of female Tettigonia viridissima to simulated bat echolocation calls were examined during tethered flight. The insects responded with three distinct behaviours, which occurred at graded stimulus intensities. At low intensities (threshold 54 dB SPL), T. viridissima responded by steering away from the sound source (negative phonotaxis). At intensities approximately 10 dB higher, beating of the hindwing was interrupted, although the insect remained in the flight posture. A diving response (cessation of the wingbeat, closure of the forewings and alignment of the legs against the body) occurred with a threshold of 76 dB SPL. Considering these thresholds, we estimate that the diving response occurs at approximately the sound amplitude at which many aerial-hawking bats first receive echoes from the insect. The other behaviours probably occur before the bat detects the insect and should therefore be interpreted as early avoidance behaviours. The repertoire of startle responses in T. viridissima, with directional and non-directional components, is similar to those of crickets and moths, but quite different from those described for another bushcricket (Neoconocephalus ensiger), which shows only a non-directional response. This supports the conclusion that bat-evasive behaviours are not conserved within the Tettigoniidae, but instead are shaped by the ecological constraints of the insects.

Male recognition mechanism for female responses implies a dilemma for their localisation in a phaneropterine bushcricket.

The phonotactic behaviour of the duetting bushcricket Poecilimon ornatus was investigated on a walking compensator when two females responded to the male's call. Whenever two female clicks from different directions were presented within the time window, males tracked an intermediate course even when the two clicks were separated by up to 60 ms and differed widely in intensity. Thus, any signal arriving within that interval contributes to the localization of the female response. The inability of male P. ornatus to selectively track one of two females is in contrast to previous results found in other bushcricket species which track the leading of two singing animals. We suggest that the intermediate walking is a consequence of the basic ensiferan neuronal processing of song recognition and localization. Choice experiments in the natural habitat show that earlier or later during the phonotactic path--the male tracks that female which is favoured by the unpredictable acoustic conditions in dense vegetation.

Listening for bats: the hearing range of the bushcricket Phaneroptera falcata for bat echolocation calls measured in the field.

The hearing range of the tettigoniid Phaneropterafalcata for the echolocation calls of freely flying mouseeared bats (Myotis myotis) was determined in the field. The hearing of the insect was monitored using hook electrode recordings from an auditory interneuron, which is as sensitive as the hearing organ for frequencies above 16 kHz. The flight path of the bat relative to the insect's position was tracked by recording the echolocation calls with two microphone arrays, and calculating the bat's position from the arrival time differences of the calls at each microphone. The hearing distances ranged from 13 to 30 m. The large variability appeared both between different insects and between different bat approaches to an individual insect. The escape time of the bushcricket, calculated from the detection distance of the insect and the instantaneous flight speed of the bat, ranged from 1.5 to more than 4s. The hearing ranges of bushcrickets suggest that the insect hears the approaching bat long before the bat can detect an echo from the flying insect.

A quantitative analysis of behavioral selectivity for pulse rise-time in the gray treefrog, Hyla versicolor.

The selectivity of female phonotactic responses to synthetic advertisement calls was tested in choice situations. Preferences based on differences in the linear rise-time of synthetic pulses depended on intensity and carrier frequency. When the carrier frequency was 1.1 kHz, simulating the low-frequency peak in the advertisement call, females preferred alternatives with slower rise-time pulses that differed by 5 ms at playback levels of 75 dB SPL and higher. A rise-time difference of 10 ms was discriminated at 65 dB SPL. When the carrier frequency was 2.2 kHz, simulating the high-frequency peak in the call, females discriminated a 5-ms difference in rise-time only at 85 dB SPL. Females showed no preference when the difference was 10 ms at lower playback levels. The difference in the thresholds (about 15-20 dB) for discriminating differences in rise-time at the two carrier frequencies was greater than the difference in behavioral thresholds for these two frequencies (about 10 dB). This result suggests that rise-time discrimination can be mediated solely by the neural channel mainly tuned to the low-frequency peak in the call. Females probably assess differences in rise-time by comparing the first few pulses of each call rather than by averaging over the entire call.

Significance of forebrain structures in acoustically guided behavior in anurans.

In order to test the hypothesis that the forebrain is involved in controlling acoustically guided behaviour, we carried out behavioural studies in combination with brain lesions, neuroanatomical and electrophysiological experiments in males and females of different species of frogs. Whereas the dorsomedial pallium plays no or only a minor role, the striatum, the septum, and the preoptic area potentially influence the behaviour because they send parallel descending projections to different premotor and motor networks in the brainstem. These parallel projections may be the basis for the variability seen in the behaviour.

Directional hearing in grasshoppers: neurophysiological testing of a bioacoustic model

A recently proposed biophysical model for directional hearing in grasshoppers was tested using complex stimulus situations, with two loudspeakers, one on either side of the animal, synchronously emitting sinusoids with defined phase and amplitude relationships. Hearing responses were determined from whole nerve recordings and compared with the predictions of the model. In Schistocerca gregaria, there were only minor differences between the predictions of the model and measurements and, by reducing the value of the gain of the internal sound path measured previously, a close agreement was achieved between model and measured hearing responses. In Chorthippus biguttulus, larger discrepancies between model calculations using the values measured previously and neuronal response functions were found in both shape and amplitude. A better fit between measurements and model predictions was achieved by increasing the values of the internal delay over those measured previously. The measurements presented here indicate high inter-individual variability of the parameters of the internal pathway, with a range of 60 degrees for the internal phase delay. Calculating the directional characteristics using this range of values for the internal delay indicated that sufficient directional information was available down to 5 kHz. Increasing the value of the internal delay over that measured in an earlier study therefore provides an explanation for the discrepancy between the poor directional information attributed to C. biguttulus in that study and the excellent lateralization ability of males of this species at 5 kHz.

Specific differences in sound production and pattern recognition in tettigoniids.

A brief comparative description of the stridulatory songs of nine different tettigoniid species is given to introduce a set of four parameters (phase of sound production during opening and closing movement of the wings, syllable repetition mode, syllable similarity, and impulse pattern of the syllables) to characterize the temporal pattern of tettigoniid songs. The importance of different song parameters for female phonotaxis was investigated in two tettigoniid species (Ephippiger ephippiger and Tettigonia viridissima). Two-choice experiments revealed that the impulse pattern of the closing syllable is an important parameter for the phonotactic behaviour of E. ephippiger, whereas the syllable pattern is a decisive parameter for species discrimination in T. viridissima.