Intraspecific acoustic communication and mechanical sensitivity of the tympanal ear of the gypsy moth Lymantria dispar

Tympanal ears of female gypsy moths Lymantria dispar dispar (L.) (Lepidoptera: Erebidae: Lymantriinae) are reportedly more sensitive than ears of conspecific males to sounds below 20 kHz. The hypothesis is tested that this differential sensitivity is a result of sex‐specific functional roles of sound during sexual communication, with males sending and females receiving acoustic signals. Analyses of sounds produced by flying males reveal a 33‐Hz wing beat frequency and 14‐kHz associated clicks, which remain unchanged in the presence of female sex pheromone. Females exposed to playback sounds of flying conspecific males respond with wing raising, fluttering and walking, generating distinctive visual signals that may be utilized by mate‐seeking males at close range. By contrast, females exposed to playback sounds of flying heterospecific males (Lymantria fumida Butler) do not exhibit the above behavioural responses. Laser Doppler vibrometry reveals that female tympana are particularly sensitive to frequencies in the range produced by flying conspecific males, including the 33‐Hz wing beat frequency, as well as the 7‐kHz fundamental frequency and 14‐kHz dominant frequency of associated clicks. These results support the hypothesis that the female L. dispar ear is tuned to sounds of flying conspecific males. Based on previous findings and the data of the present study, sexual communication in L. dispar appears to proceed as: (i) females emitting sex pheromone that attracts males; (ii) males flying toward calling females; and (iii) sound signals from flying males at close range inducing movement in females, which, in turn, provides visual signals that could orient males toward females.     

Female frog auditory sensitivity,male calls,and background noise: potential influences on the evolution of a peculiar matched filter

The matched filter hypothesis proposes that the tuning of females' auditory sensitivity matches the spectral energy distribution of males' signals. Such correspondence is expected to arise over evolutionary time, as it promotes conspecific information transfer and reduces interference from other sound sources. Our main objective was to determine the correspondence between the acoustic sensitivity of female frogs of Eupsophus roseus and the spectral characteristics of advertisement vocalizations produced by conspecific males. We also aimed to determine how auditory sensitivity is related to the characteristics of background noise. We analysed data on the auditory sensitivity of E. roseus females, and recordings of conspecific male vocalizations and of the acoustic environment during the breeding period of this species. Our results indicate a concordance between the auditory sensitivity of females and call spectra that would provide an appropriate detection of these signals. In addition, this matching is large relative to the correspondence between auditory sensitivity with the spectra of the abiotic and biotic background noise, with the last component being associated with calls of the related species Eupsophus vertebralis. This may be an adaptation of receivers confronting sound interference, which improves the capability of E. roseus to communicate sexually by means of acoustic signals. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 814–827.     

Neural mechanisms of auditory species recognition in birds

Auditory communication in humans and other animals frequently takes place in noisy environments with many co‐occurring signallers. Receivers are thus challenged to rapidly recognize salient auditory signals and filter out irrelevant sounds. Most bird species produce a variety of complex vocalizations that function to communicate with other members of their own species and behavioural evidence broadly supports preferences for conspecific over heterospecific sounds (auditory species recognition). However, it remains unclear whether such auditory signals are categorically recognized by the sensory and central nervous system. Here, we review 53 published studies that compare avian neural responses between conspecific versus heterospecific vocalizations. Irrespective of the techniques used to characterize neural activity, distinct nuclei of the auditory forebrain are consistently shown to be repeatedly conspecific selective across taxa, even in response to unfamiliar individuals with distinct acoustic properties. Yet, species‐specific neural discrimination is not a stereotyped auditory response, but is modulated according to its salience depending, for example, on ontogenetic exposure to conspecific versus heterospecific stimuli. Neuromodulators, in particular norepinephrine, may mediate species recognition by regulating the accuracy of neuronal coding for salient conspecific stimuli. Our review lends strong support for neural structures that categorically recognize conspecific signals despite the highly variable physical properties of the stimulus. The available data are in support of a ‘perceptual filter’‐based mechanism to determine the saliency of the signal, in that species identity and social experience combine to influence the neural processing of species‐specific auditory stimuli. Finally, we present hypotheses and their testable predictions, to propose next steps in species‐recognition research into the emerging model of the neural conceptual construct in avian auditory recognition.     

An exception to the matched filter hypothesis: A mismatch of male call frequency and female best hearing frequency in a torrent frog

The matched filter hypothesis proposes that the tuning of auditory sensitivity and the spectral character of calls will match in order to maximize auditory processing efficiency during courtship. In this study, we analyzed the acoustic structure of male calls and both male and female hearing sensitivities in the little torrent frog (Amolops torrentis), an anuran species who transmits acoustic signals across streams. The results were in striking contradiction to the matched filter hypothesis. Auditory brainstem response results showed that the best hearing range was 1.6–2 kHz consistent with the best sensitive frequency of most terrestrial lentic taxa, yet completely mismatched with the dominant frequency of conspecific calls (4.3 kHz). Moreover, phonotaxis tests show that females strongly prefer high‐frequency (4.3 kHz) over low‐frequency calls (1.6 kHz) regardless of ambient noise levels, although peripheral auditory sensitivity is highest in the 1.6–2 kHz range. These results are consistent with the idea that A. torrentis evolved from nonstreamside species and that high‐frequency calls evolved under the pressure of stream noise. Our results also suggest that female preferences based on central auditory system characteristics may evolve independently of peripheral auditory system sensitivity in order to maximize communication effectiveness in noisy environments.     

Adult female hamsters require long and sustained exposures to heterospecific males to avoid interspecific mating

Interspecific mating normally decreases female fitness. In many species, females avoid heterospecific males innately or by imprinting on their parents. Alternatively, adult females could learn to discriminate against heterospecific males after exposure to such males. For example, Syrian hamster (Mesocricetus auratus) females learn to discriminate between conspecific males and Turkish hamster (M. brandti) males during adulthood by exposure to males of both species. Adult females not previously exposed to Turkish hamster males will mate similarly with conspecific and heterospecific males. However, in a previous study we showed that exposure to a heterospecific male and a conspecific male for 8 days led to mating avoidance and aggression towards the heterospecific male. Here we conducted two experiments to investigate how much exposure to the heterospecific male was required for females to avoid mating with the heterospecific male (Experiment 1) and how long that avoidance lasted in the absence of continuous exposure to heterospecific stimuli (Experiment 2). Fast and durable learning would indicate the evolution of an efficient avoidance response. In Experiment 1, females were exposed to a heterospecific male for 1, 4 h, 4 or 8 days and then paired with that male. We found more avoidance of interspecific mating after 4 or 8 days of exposure than after 1 or 4 h of exposure. In Experiment 2, females were exposed to a heterospecific male for 8 days and then paired with that male either 10 min later or 8 days later. We found that after an 8-day delay females were highly sexually receptive to the heterospecific male. Additionally, a comparison between the current experiments and a previous study indicates that female Syrian hamsters do not require concurrent exposure to a conspecific male and a heterospecific male to learn to avoid interspecific mating; exposure to a heterospecific male is sufficient.     

Reproductive interference by male Drosophila subobscura on female D. persimilis: A laboratory experiment

While females often reject courtship attempts by heterospecific males, reproductive interference by harassment from such males can nonetheless occur, potentially reducing female fitness. Such effects may be profound following a range expansion, when males from a new species may suddenly encounter (and perhaps even become abundant relative to) females of related native species. Drosophila subobscura recently invaded North America and may impact native species through reproductive interference and other processes. We test for the potential for reproductive interference by D. subobscura males on D. persimilis females in the laboratory. D. subobscura males aggressively copulated with D. persimilis females, including many females that exhibit rejection behaviors. Despite females attempting to dismount the males, the heterospecific copulations are on average longer than conspecific copulations, and females exhibit some reluctance to remate with conspecific males following this harassment. Females confined with both conspecific and heterospecific males produce fewer adult progeny than those with either conspecific males only or with conspecific males and distantly related D. simulans males that do not engage in female harassment. Overall, our results illustrate how reproductive interference by an invasive species can have negative effects on resident natural populations.     

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko,Gekko subpalmatus

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects’ vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.     

Acoustic orientation of male Aedes diantaeus during mating

The reaction of males of Aedes diantaeus to different auditory stimuli was studied in natural environment during swarming and under laboratory conditions. The males were attracted by 250-420 Hz that corresponds to the main frequencies of flight tones of sympatric females and the range of sensitivity of male Johnston's organs. Behavioural data show that in natural environment swarming males are attracted by flying conspecific and heterospecific females rather than by dead or immobilized females. Contact with heterospecific females always ended in parting of mosquitoes while contact with cospecific females resulted in pairing. Thus, swarming males of Aedes diantaeus localize females by their flight tones but recognize the females of their own species in contact.     

Developmental experience alters information coding in auditory midbrain and forebrain neurons

In songbirds, species identity and developmental experience shape vocal behavior and behavioral responses to vocalizations. The interaction of species identity and developmental experience may also shape the coding properties of sensory neurons. We tested whether responses of auditory midbrain and forebrain neurons to songs differed between species and between groups of conspecific birds with different developmental exposure to song. We also compared responses of individual neurons to conspecific and heterospecific songs. Zebra and Bengalese finches that were raised and tutored by conspecific birds, and zebra finches that were cross‐tutored by Bengalese finches were studied. Single‐unit responses to zebra and Bengalese finch songs were recorded and analyzed by calculating mutual information (MI), response reliability, mean spike rate, fluctuations in time‐varying spike rate, distributions of time‐varying spike rates, and neural discrimination of individual songs. MI quantifies a response's capacity to encode information about a stimulus. In midbrain and forebrain neurons, MI was significantly higher in normal zebra finch neurons than in Bengalese finch and cross‐tutored zebra finch neurons, but not between Bengalese finch and cross‐tutored zebra finch neurons. Information rate differences were largely due to spike rate differences. MI did not differ between responses to conspecific and heterospecific songs. Therefore, neurons from normal zebra finches encoded more information about songs than did neurons from other birds, but conspecific and heterospecific songs were encoded equally. Neural discrimination of songs and MI were highly correlated. Results demonstrate that developmental exposure to vocalizations shapes the information coding properties of songbird auditory neurons. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 70: 235–252, 2010.     

Candidate neural locus for sex differences in reproductive decisions

Sexual selection and signal detection theories predict that females should be selective in their responses to mating signals in mate choice, while the response of males to signals in male competition should be less selective. The neural processes underlying this behavioural sex difference remain obscure. Differences in behavioural selectivity could result from differences in how sensitive sensory systems are to mating signals, distinct thresholds in motor areas regulating behaviour, or sex differences in selectivity at a gateway relaying sensory information to motor systems. We tested these hypotheses in frogs using the expression of egr-1 to quantify the neural responses of each sex to mating signals. We found that egr-1 expression in a midbrain auditory region was elevated in males in response to both conspecific and heterospecific calls, whereas in females, egr-1 induction occurred only in response to conspecific signals. This differential neural selectivity mirrored the sex differences in behavioural responsiveness to these stimuli. By contrast, egr-1 expression in lower brainstem auditory centres was not different in males and females. Our results support a model in which sex differences in behavioural selectivity arise from sex differences in the neural selectivity in midbrain areas relaying sensory information to the forebrain.     

Male recognition of conspecific female chemical cues in a diverse clade of freshwater fishes

Where orangethroat darters (Etheostoma: Ceasia) and rainbow darters (Etheostoma caeruleum) co-occur, males prefer conspecific over heterospecific females. The cues males use to identify conspecific females remain unclear. We conducted behavioral trials to ask whether chemical cues function in conspecific recognition. We found that males from three orangethroat darter species preferentially associate with female scent over a control. Our results support the use of olfaction in conspecific identification in the orangethroat clade and contribute to our understanding of signals that may facilitate species recognition and underlie the evolution of behavioral isolation.     

Drosophila melanogaster males respond differently at the behavioural and genome‐wide levels to Drosophila melanogaster and Drosophila simulans females

Drosophila melanogaster are found in sympatry with Drosophila simulans, and matings between the species produce nonfertile hybrid offspring at low frequency. Evolutionary theory predicts that females choose mates, so males should alter their behaviour in response to female cues. We show that D. melanogaster males quickly decrease courtship towards D. simulans females. Courtship levels are reduced within 5 min of exposure to a heterospecific female, and overall courtship is significantly lower than courtship towards conspecific females. To understand changes at the molecular level during mate choice, we performed microarray analysis on D. melanogaster males that courted heterospecific D. simulans females and found nine genes have altered expression compared with controls. In contrast, males that court conspecific females alter expression of at least 35 loci. The changes elicited by conspecific courtship likely modulate nervous system function to reinforce positive conspecific signals and dampen the response to heterospecific signals.     

REPRODUCTIVE BEHAVIOR OF FEMALE BUNTINGS: ISOLATING MECHANISMS IN A HYBRIDIZING PAIR OF SPECIES

The plumage characteristics of male Indigo and Lazuli Buntings are distinct, but the two species can learn each other's songs. Populations comprising Indigo, Lazuli and hybrid individuals occur in the Great Plains of North America, and assortative mating has been inferred from morphometric data. We devised a laboratory assay for determining female preferences for visual and vocal characteristics of conspecific and heterospecific males and for mixtures of these characteristics, such as might be encountered in an overlap population. Females of both species gave more copulation-solicitation displays when exposed to conspecific plumage and vocalizations than when exposed to heterospecific plumage and vocalizations. Females gave intermediate and similar responses to the combinations of conspecific plumage with heterospecific vocalizations and heterospecific plumage with conspecific vocalizations. Thus, in the absence of other potentially important variables, female reproductive behavior is consistent with the hypothesis of assortative mating, based upon both vocal and visual traits of the males and caused by female choice in this semispecies pair.     

Auditory temporal resolution and evoked responses to pulsed sounds for the Yangtze finless porpoises (<Emphasis Type="Italic">Neophocaena phocaenoides asiaeorientalis</Emphasis>)

Temporal cues are important for some forms of auditory processing, such as echolocation. Among odontocetes (toothed whales, dolphins, and porpoises), it has been suggested that porpoises may have temporal processing abilities which differ from other odontocetes because of their relatively narrow auditory filters and longer duration echolocation signals. This study examined auditory temporal resolution in two Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) using auditory evoked potentials (AEPs) to measure: (a) rate following responses and modulation rate transfer function for 100 kHz centered pulse sounds and (b) hearing thresholds and response amplitudes generated by individual pulses of different durations. The animals followed pulses well at modulation rates up to 1,250 Hz, after which response amplitudes declined until extinguished beyond 2,500 Hz. The subjects had significantly better hearing thresholds for longer, narrower-band pulses similar to porpoise echolocation signals compared to brief, broadband sounds resembling dolphin clicks. Results indicate that the Yangtze finless porpoise follows individual acoustic signals at rates similar to other odontocetes tested. Relatively good sensitivity for longer duration, narrow-band signals suggests that finless porpoise hearing is well suited to detect their unique echolocation signals.     

Neural correlates of threat perception: neural equivalence of conspecific and heterospecific mobbing calls is learned

Songbird auditory areas (i.e., CMM and NCM) are preferentially activated to playback of conspecific vocalizations relative to heterospecific and arbitrary noise. Here, we asked if the neural response to auditory stimulation is not simply preferential for conspecific vocalizations but also for the information conveyed by the vocalization. Black-capped chickadees use their chick-a-dee mobbing call to recruit conspecifics and other avian species to mob perched predators. Mobbing calls produced in response to smaller, higher-threat predators contain more "D" notes compared to those produced in response to larger, lower-threat predators and thus convey the degree of threat of predators. We specifically asked whether the neural response varies with the degree of threat conveyed by the mobbing calls of chickadees and whether the neural response is the same for actual predator calls that correspond to the degree of threat of the chickadee mobbing calls. Our results demonstrate that, as degree of threat increases in conspecific chickadee mobbing calls, there is a corresponding increase in immediate early gene (IEG) expression in telencephalic auditory areas. We also demonstrate that as the degree of threat increases for the heterospecific predator, there is a corresponding increase in IEG expression in the auditory areas. Furthermore, there was no significant difference in the amount IEG expression between conspecific mobbing calls or heterospecific predator calls that were the same degree of threat. In a second experiment, using hand-reared chickadees without predator experience, we found more IEG expression in response to mobbing calls than corresponding predator calls, indicating that degree of threat is learned. Our results demonstrate that degree of threat corresponds to neural activity in the auditory areas and that threat can be conveyed by different species signals and that these signals must be learned.     

Representation of complex vocalizations in the Lusitanian toadfish auditory system: evidence of fine temporal,frequency and amplitude discrimination

Many fishes rely on their auditory skills to interpret crucial information about predators and prey, and to communicate intraspecifically. Few studies, however, have examined how complex natural sounds are perceived in fishes. We investigated the representation of conspecific mating and agonistic calls in the auditory system of the Lusitanian toadfish Halobatrachus didactylus, and analysed auditory responses to heterospecific signals from ecologically relevant species: a sympatric vocal fish (meagre Argyrosomus regius) and a potential predator (dolphin Tursiops truncatus). Using auditory evoked potential (AEP) recordings, we showed that both sexes can resolve fine features of conspecific calls. The toadfish auditory system was most sensitive to frequencies well represented in the conspecific vocalizations (namely the mating boatwhistle), and revealed a fine representation of duration and pulsed structure of agonistic and mating calls. Stimuli and corresponding AEP amplitudes were highly correlated, indicating an accurate encoding of amplitude modulation. Moreover, Lusitanian toadfish were able to detect T. truncatus foraging sounds and A. regius calls, although at higher amplitudes. We provide strong evidence that the auditory system of a vocal fish, lacking accessory hearing structures, is capable of resolving fine features of complex vocalizations that are probably important for intraspecific communication and other relevant stimuli from the auditory scene.     

Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders

Jumping spiders (Salticidae) are renowned for their exceptional vision, but this does not preclude use of other senses. Here we provide evidence that olfactory pheromones are widespread in the Spartaeinae and Lyssomaninae, two subfamilies regarded as basal clades within the Salticidae. Pheromone use by salticids was tested in a series of experiments: males were tested with the odour of conspecific females, heterospecific females, and conspecific males, and females were tested with the odour of conspecific males. With seven of the 29 species tested, we also tested males using the draglines of conspecific females (spider absent) as the odour source. Males of all species tested were attracted to the odour of conspecific females and to the odour of the draglines of conspecific females. There was no evidence of males responding to the odour of heterospecific females or conspecific males, or of females responding to the odour of conspecific males. These findings suggest that it is primarily males that respond to olfactory sex pheromones, consistent with the apparent trend within spiders of males more actively searching for females and females placing greater emphasis on mate‐choice decisions. Compared with most salticid groups, lyssomanines and spartaeines are unusually sedentary and this lifestyle may favour olfactory mate searching. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 664–677.     

Acoustic signal perception in a noisy habitat: lessons from synchronising insects

Acoustically communicating animals often have to cope with ambient noise that has the potential to interfere with the perception of conspecific signals. Here we use the synchronous display of mating signals in males of the tropical katydid Mecopoda elongata in order to assess the influence of nocturnal rainforest noise on signal perception. Loud background noise may disturb chorus synchrony either by masking the signals of males or by interaction of noisy events with the song oscillator. Phase-locked synchrony of males was studied under various signal-to-noise ratios (SNRs) using either native noise or the audio component of noise (<9 kHz). Synchronous entrainment was lost at a SNR of -3 dB when native noise was used, whereas with the audio component still 50% of chirp periods matched the pacer period at a SNR of -7 dB. Since the chirp period of solo singing males remained almost unaffected by noise, our results suggest that masking interference limits chorus synchrony by rendering conspecific signals ambiguous. Further, entrainment with periodic artificial signals indicates that synchrony is achieved by ignoring heterospecific signals and attending to a conspecific signal period. Additionally, the encoding of conspecific chirps was studied in an auditory neuron under the same background noise regimes.     

SEXUALLY MONOMORPHIC MATING PREFERENCES CONTRIBUTE TO PREMATING ISOLATION BASED ON SONG IN EUROPEAN GREEN LACEWINGS

When species are in intermediate stages of divergence, complicated patterns of reproductive isolation can arise among males and females of the incipient species. The Chrysoperla carnea group of green lacewings (Neuroptera: Chrysopidae) has recently experienced rapid speciation. They possess sexually monomorphic mating signals that were assumed to be important in mate recognition. Our objective was to compare patterns of reproductive isolation among five European species within the species complex as well as sex differences in mating strategies that contribute to those patterns. The species were in fact reproductively isolated based on mating signals. In addition, different species showed different degrees of responsiveness to conspecific signals, and those species that responded more frequently to conspecific signals were less discriminating against heterospecific signals. This suggests differences in mating strategies among species that may be related to population densities and heterospecific encounter rates. Sexual dimorphism in mating preference was apparent only in C. agilis , whose males were more responsive to all signals and less discriminating against heterospecific signals compared to females. Thus high variance in male quality may be characteristic of C. agilis , but not the remaining four species, whose male versus female mating strategies were similar.     

Auditory saccular sensitivity of the vocal Lusitanian toadfish: low frequency tuning allows acoustic communication throughout the year

A novel form of auditory plasticity for enhanced detection of social signals was described in a teleost fish, Porichthys notatus (Batrachoididae, Porichthyinae). The seasonal onset of male calling coincides with inshore migration from deep waters by both sexes and increased female sensitivity to dominant frequencies of male calls. The closely related Lusitanian toadfish, Halobatrachus didactylus, (Batrachoididae, Halophryninae) also breeds seasonally and relies on acoustic communication to find mates but, instead, both sexes stay in estuaries and show vocal activity throughout the year. We investigated whether the sensitivity of the inner ear saccule of H. didactylus is seasonally plastic and sexually dimorphic. We recorded evoked potentials from populations of saccular hair cells from non-reproductive and reproductive males and females in response to 15–945 Hz tones. Saccular hair cells were most sensitive at 15–205 Hz (thresholds between 111 and 118 dB re. 1 μPa). Both sexes showed identical hearing sensitivity and no differences were found across seasons. The saccule was well suited to detect conspecific vocalizations and low frequencies that overlapped with lateral line sensitivity. We showed that the saccule in H. didactylus has major importance in acoustic communication throughout the year and that significant sensory differences may exist between the two batrachoidid subfamilies.