Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs

Advertisement calls of closely related species often differ in quantitative features such as the repetition rate of signal units. These differences are important in species recognition. Current models of signal-receiver coevolution predict two possible patterns in the evolution of the mechanism used by receivers to recognize the call: (i) classical sexual selection models (Fisher process, good genes/indirect benefits, direct benefits models) predict that close relatives use qualitatively similar signal recognition mechanisms tuned to different values of a call parameter; and (ii) receiver bias models (hidden preference, pre-existing bias models) predict that if different signal recognition mechanisms are used by sibling species, evidence of an ancestral mechanism will persist in the derived species, and evidence of a pre-existing bias will be detectable in the ancestral species. We describe qualitatively different call recognition mechanisms in sibling species of treefrogs. Whereas Hyla chrysoscelis uses pulse rate to recognize male calls, Hyla versicolor uses absolute measurements of pulse duration and interval duration. We found no evidence of either hidden preferences or pre-existing biases. The results are compared with similar data from katydids (Tettigonia sp.). In both taxa, the data are not adequately explained by current models of signal-receiver coevolution.     

Mid-frequency suppression in the green treefrog (<Emphasis Type="Italic">Hyla cinerea</Emphasis>): mechanisms and implications for the evolution of acoustic communication

Advertisement calls of green treefrogs (Hyla cinerea) have two spectral peaks centered at about 1 kHz and 3 kHz. Addition of a component of intermediate frequency (1.8 kHz) to a synthetic call reduced its attractiveness to females relative to an alternative lacking this component. This mid-frequency suppression occurred over a 20-dB range of playback levels. Addition of other intermediate frequencies had weak effects on preferences at some playback levels, in some localities, and at lower-than-normal temperatures. These effects correlate well with the response properties of a population of low-frequency-tuned auditory neurons innervating the amphibian papilla. Males of a closely related species (H. gratiosa) produce calls with emphasized frequencies within the range of suppression in H. cinerea; however, suppression also occurred in localities well outside the area of geographical overlap with this species. Thus, previous speculation that mid-frequency suppression evolved to enhance species discrimination is probably incorrect. This phenomenon is more likely to reflect a general sensory bias in anurans and other vertebrates, tone-on-tone inhibition. Such negative biases, and other inhibitory mechanisms, almost certainly play an important role in the evolution of communication systems but have received far less attention than positive biases that enhance signal attractiveness.     

Female reproductive state influences the auditory midbrain response

Female behavioral responses to sensory stimuli can be highly variable across the reproductive cycle. Female green treefrogs (Hyla cinerea) use the male vocal signal to locate and choose a mate. Gravid females approach a vocalizing male to mate but do not approach if they have recently mated. Such differences in behavioral response may be due in part to shifts in the neural representation of auditory information in the brain. In this study, we investigated the influence of female reproductive state on neural responses in the auditory midbrain to both communication signals (advertisement calls) and non-communication sounds (band limited noise bursts). Recently mated females exhibited significantly reduced response strengths compared to females not recently mated. Reduced response strengths in post-mated females were in response to both noise bursts and male advertisement calls but were limited to the lower frequency range corresponding to the amphibian papilla of the peripheral auditory system. Our results therefore show that the ability of social signals to stimulate the auditory system differs in females depending on their reproductive state, and that the differential effect on low versus high spectral sensitivities may influence the way the two spectral peaks of male advertisement calls are represented.     

Modeling and computational analysis of EGF receptor-mediated cell communication in Drosophila oogenesis

Autocrine signaling through the Epidermal Growth Factor Receptor (EGFR) operates at various stages of development across species. A recent hypothesis suggested that a distributed network of EGFR autocrine loops was capable of spatially modulating a simple single-peaked input into a more complex two-peaked signaling pattern, specifying the formation of a pair organ in Drosophila oogenesis (two respiratory appendages on the eggshell). To test this hypothesis, we have integrated genetic and biochemical information about the EGFR network into a mechanistic model of transport and signaling. The model allows us to estimate the relative spatial ranges and time scales of the relevant feedback loops, to interpret the phenotypic transitions in eggshell morphology and to predict the effects of new genetic manipulations. We have found that the proposed mechanism with a single diffusing inhibitor is sufficient to convert a single-peaked extracellular input into a two-peaked pattern of intracellular signaling. Based on extensive computational analysis, we predict that the same mechanism is capable of generating more complex patterns. At least indirectly, this can be used to account for more complex eggshell morphologies observed in related fly species. We propose that versatility in signaling mediated by autocrine loops can be systematically explored using experiment-based mechanistic models and their analysis.     

Changes in the Frequency Structure of a Mating Call Decrease Its Attractiveness to Females in the Cricket Frog Acris crepitans blanchardi

In many species, females often prefer male signals that are more complex than in nature or beyond the range of calls naturally produced by conspecific males in spectral, temporal and amplitude features. In this study we examined both the ability of females to recognize signals outside the normal range of spectral frequency variation seen in male advertisement calls, and the influence of increasing call complexity by adding spectral components to enhance the attractiveness of a male advertisement call in the cricket frog Acris crepitans blanchardi, while keeping its amplitude constant. We used two different natural male call groups and created the following synthetic call groups: with a dominant frequency at 3500 Hz, i.e. at the normal dominant frequency with a frequency band within the sensitivity range of the inner ear basilar papilla; with a dominant frequency at 700 Hz, i.e. outside the normal range of variation and with a frequency band outside the sensitivity range of the basilar papilla but within the range of the amphibian papilla; with two dominant frequencies, one at 700 Hz and another at 3500 Hz, stimulating the basilar and amphibian papilla simultaneously. In double choice experiments we tested all combinations of the three call groups, and we tested the 3500 Hz call groups against the same natural call groups. Additionally, we tested the 700 Hz call groups against white noise to see whether these signals are meaningful in mate choice. Females preferred 3500 Hz call groups over all other call groups. The synthetic call group was as attractive to females as the same natural call group. The 700 Hz call group was not meaningful in mate choice. The combined (700 Hz + 3500 Hz) call group was significantly less attractive to females than the 3500 Hz call group. Thus, making a call more spectrally complex without increasing its overall amplitude decreases its attractiveness to cricket frog females.     

THE FUNCTION OF CALL ALTERNATION IN ANURAN AMPHIBIANS: A TEST OF THREE HYPOTHESES

Males of many species of anurans alternate calls with those of their neighbors in a chorus. This pattern of calling reduces signal interference and may: 1) facilitate intermale spacing because males can better gauge the intensity of neighbors' calls if these calls do not overlap with their own; 2) help preserve species-specific temporal information in calls required to attract females; and/or 3) make it easier for females to localize males in the chorus. I tested these hypotheses with three species that exhibit call alternation, Hyla crucifer, H. versicolor, and H. microcephala. Males of all three species gave more aggressive calls to high-intensity synthetic stimuli that alternated with their calls than to those that overlapped their calls. These results support the first hypothesis. Results of four-speaker female choice experiments using alternating and overlapping calls indicate that preservation of signal integrity also is important in H. versicolor and H. microcephala, species that have fine-scale temporal information in their calls. However, the third hypothesis was not supported; females failed to discriminate among alternating and overlapping calls if the problem of signal disruption was eliminated or irrelevant.     

Co-option of male courtship signals from aggressive display in bowerbirds

The pre-existing trait hypothesis suggests that females evolve a mating preference for an already existing male trait. This hypothesis poses a simple resolution to Darwin's long-standing question of how elaborate, male display traits evolve. The frequently observed convergence of aggressive and courtship displays across a wide array of species provides the only current support for this hypothesis. Here we provide much more detailed supporting evidence from bowerbird skrraa calls used in aggression and courtship. Consistent with the pre-existing trait hypothesis we show that (i) putatively co-opted skrraa calls used in courtship and aggression are homologous, (ii) skrraa calls were used in aggression in bowerbirds before being used in courtship, (iii) historically, intense, aggressive-like courtship calls were present near the time of co-option, and (iv) bower types contemporaneous with co-option emphasize design features that provide females protection from the adverse effects of intense courtship displays. These results, plus evidence for a female preference for males with intense aggressive-like courtship skrraa calls, suggest that aggressive skrraa calls have been co-opted for use in male courtship display     

Has the evolution of complexity in the amphibian papilla influenced anuran speciation rates?

For anurans, increasing complexity of the inner ear has been correlated with speciation rates. The evolution of a complex amphibian papilla (AP) is thought to have facilitated speciation by extending the range of frequencies over which mating calls may diverge. Although this example has been proposed to represent a key innovation, the mechanism by which the AP is thought to promote speciation makes the questionable assumption that anurans generally use the AP for detection of their mating calls. This study uses mating calls from 852 species to test this assumption. Surprisingly, the calls of most species are not detected by the AP but by a second organ, the basilar papilla (BP). This refutes the role of AP complexity in facilitating call divergence and hence, speciation. Future research into the evolution of acoustically mediated reproductive isolation should focus instead on the BP as it may play a more critical role in anuran speciation.     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

Seasonal plasticity in auditory processing of the envelope and temporal fine structure of sounds in three songbirds

Songs mediate mate attraction and territorial defence in songbirds during the breeding season. Outside of the breeding season, the avian vocal repertoire often includes calls that function in foraging, antipredator and social behaviours. Songs and calls can differ substantially in their spectral and temporal content. Given seasonal variation in the vocal signals, the sender–receiver matching hypothesis predicts seasonal changes in auditory processing that match the physical properties of songs during the breeding season and calls outside of it. We tested this hypothesis in white-breasted nuthatches, Sitta carolinensis, tufted titmice, Baeolophus bicolor, and Carolina chickadees, Poecile carolinensis. We measured the envelope-following response (EFR), which quantifies phase locking to the amplitude envelope, and the frequency-following response (FFR), which quantifies phase locking to the temporal fine structure of sounds. Because songs and calls of nuthatches are amplitude modulated at different rates, we predicted seasonal changes in EFRs that match the rates of amplitude fluctuation in songs and calls. In chickadees and titmice, we predicted stronger FFRs during the spring and stronger EFRs during the winter because songs are tonal and calls include amplitude-modulated elements. In all three species, we found seasonal changes in EFRs and FFRs. EFRs varied across seasons and matched the amplitude modulations of songs and calls in nuthatches. In addition, female chickadees had stronger EFRs in the winter than in the spring. In all three species, FFRs during the spring tended to be stronger in females than in males. We also found species differences in EFRs and FFRs in both seasons; EFRs and FFRs tended to be higher in nuthatches than in chickadees and titmice. We discuss the potential mechanisms underlying seasonality in EFRs and FFRs and the implications of our results for communication during the breeding season and outside of it, when these three species form mixed-species flocks.     

A sensory bias has triggered the evolution of egg-spots in cichlid fishes

Although, generally, the origin of sex-limited traits remains elusive, the sensory exploitation hypothesis provides an explanation for the evolution of male sexual signals. Anal fin egg-spots are such a male sexual signal and a key characteristic of the most species-rich group of cichlid fishes, the haplochromines. Males of about 1500 mouth-brooding species utilize these conspicuous egg-dummies during courtship--apparently to attract females and to maximize fertilization success. Here we test the hypothesis that the evolution of haplochromine egg-spots was triggered by a pre-existing bias for eggs or egg-like coloration. To this end, we performed mate-choice experiments in the basal haplochromine Pseudocrenilabrus multicolor, which manifests the plesiomorphic character-state of an egg-spot-less anal fin. Experiments using computer-animated photographs of males indeed revealed that females prefer images of males with virtual ('in-silico') egg-spots over images showing unaltered males. In addition, we tested for color preferences (outside a mating context) in a phylogenetically representative set of East African cichlids. We uncovered a strong preference for yellow, orange or reddish spots in all haplochromines tested and, importantly, also in most other species representing more basal lines. This pre-existing female sensory bias points towards high-quality (carotenoids-enriched) food suggesting that it is adaptive.     

Invasion of the acoustic niche: variable responses by native species to invasive American bullfrog calls

Biological invasions are a major threat to biodiversity. Invasive species that use acoustic communication can affect native species through interference in the acoustic niche. The American Bullfrog Lithobates catesbeianus is a highly invasive anuran that is widely distributed in the Brazilian Atlantic Rainforest. Adult male bullfrogs emit loud advertisement calls at frequencies that overlap with the calls of several native species of frogs. Given that spectral overlap is a major factor in acoustic masking, the purpose of this study was to test the effects of the acoustic invasion of L. catesbeianus on native frogs that have calls with and without spectral overlap with the invader. In field experiments, we exposed calling males of two overlapping species and two non-overlapping species to recorded bullfrog vocalizations, white noise, and the vocalization of another native frog species. To identify effects, we compared calls recorded before, during, and after exposure. Our results showed that native species altered their calls in response to the bullfrog calls. However, we also observed similar responses to white noise and heterospecific native calls. Both the invasive and heterospecific calls were emitted at low frequencies, which suggests that the observed responses might be specific to low-frequency calls. Our results provide evidence that the introduction of new sounds can cause native species to modify their calls, and that responses to exogenous sounds are species- and stimulus-specific.     

Acoustic Competition in Male Midwife Toads Alytes obstetricans and Alytes cisternasii: Response to Neighbor Size and Calling Rate. Implications for Female Choice

Effects of neighbor on male calling behavior was studied through playback experiments of synthetic calls to males of two species of midwife toads. The responses of resident males were scored considering two temporal parameters (call duration and calling rate) and one spectral parameter (dominant frequency). The sounds used for the playback tests included two levels of fundamental frequency (correlated with male size) and two levels of call repetition rate. In both species, resident males only changed their calling rate in the presence of an intruder, and the response was different for synthetic calls with two levels of dominant frequencies and with two calling rates. Resident size was not significantly correlated with the magnitude of the change in the calling rate. On the other hand, resident calling rate was significantly and positively correlated with the magnitude of the increase in calling rate of the stimulus. The maximum relative increase in calling rate was observed in A. cisternasii. In phonotaxis tests, females are preferentially attracted to calls emitted at a higher rate confirming the importance of changes in calling rate for female attraction.     

Evolutionary and neurobiological implications of selective phonotaxis in the spring peeper (Hyla crucifer)

Males of the spring peeper (Hyla crucifer) in central Missouri produce frequency-modulated, sinusoidal advertisement calls with a duration of 90–250 ms, and a mid-point frequency of 2800–3360 Hz. The frequency of the call is inversely correlated with body size. In playback experiments with synthetic stimuli, females did not prefer a frequency-modulated call to a call of constant frequency. Females preferred a call with a duration of 150 ms to sounds with durations of 40, 75 and 400 ms; a call of 300 ms was just as attractive as the 150-ms call. Females preferred a call of 2875 Hz to alternatives of 4000 Hz and 2600 Hz. The auditory system of H. crucifer is thus only roughly tuned to the temporal and spectral properties of the advertisement call. The female's specificity with respect to duration alone is adequate for species recognition, but intraspecific mate choice based on call frequency is extremely unlikely.     

Did sexually dimorphic dorsal coloration evolve by a pre-existing bias in males in the lizard Sceloporus minor?

Theory and empirical evidence indicate that male secondary sex traits can evolve by co-option of pre-existing biases in females. However, relatively few studies have explored whether male pre-existing biases could drive the evolution of traits important in male contests. Male spiny lizards (Sceloporus) are characterized by the expression of sexually dimorphic blue throat and abdominal patches. These features are revealed to conspecifics during social interactions, and variation in ventral color can predict the outcome of male contests in some species of spiny lizards. In Sceloporus minor, males in some populations also express bright blue color on the dorsal surfaces. Given the significance of blue color in intrasexual signaling in other species of Sceloporus, blue dorsal color may have evolved in S. minor by co-option of a male sensory bias for the color blue. We tested this hypothesis in a population that exhibits an ancestral phenotype for male dorsal color (brown/orange), and lacks males with bright blue dorsal coloration. Resident territorial males were presented with one of three types of intruder males manipulated in dorsal color by painting. Orange males mimicked the ancestral dorsal phenotype found at the study site; blue males resembled those from a population with the derived (blue) form of this trait; and green males represented a novel stimulus control. If blue dorsal color evolved in S. minor in part due to co-option of a male sensory bias, we predicted that resident males would exhibit either increased or decreased levels of aggression to blue intruders relative to controls. We found no difference in resident aggressive behavior across all treatments, thus failing to support the predictions of a pre-existing bias. We discuss these findings in the context of social behavior in Sceloporus, and propose directions for further study in this species.     

A test of the matched filter hypothesis in two sympatric frogs,Chiromantis doriae and Feihyla vittata

The matched filter hypothesis proposes that the auditory sensitivity of receivers should match the spectral energy distribution of the senders’ signals. If so, receivers should be able to distinguish between species-specific and hetero-specific signals. We tested the matched filter hypothesis in two sympatric species, Chiromantis doriae and Feihyla vittata, whose calls exhibit similar frequency characters and that overlap in the breeding season and microenvironment. For both species, we recorded male calls and measured the auditory sensitivity of both sexes using the auditory brainstem response (ABR). We compared the auditory sensitivity with the spectral energy distribution of the calls of each species and found that (1) auditory sensitivity matched the signal spectrogram in C. doriae and F. vittata; (2) the concordance conformed better to the conspecific signal versus the hetero-specific signal. In addition, our results show that species differences are larger than sex differences for ABR audiograms.     

Detection and discrimination of natural calls in masking noise by birds: estimating the active space of a signal

We tested the ability of birds to detect and discriminate natural vocal signals in the presence of masking noise using operant conditioning. Masked thresholds were measured for budgerigars, Melopsittacus undulatus, and zebra finches, Taeniopygia guttata, on natural contact calls of budgerigars, zebra finches and canaries, Serinus canaria. Thresholds increased with increasing call bandwidth, the presence of amplitude modulation and high rates of frequency modulation in calls. As expected, detection thresholds increased monotonically with background noise level. Call detection thresholds varied with the spectral shape of noise. Vocal signals were masked predominantly by noise energy in the spectral region of the signals and not by energy at spectral regions remote from the signals. In all cases, thresholds for discrimination between calls of the same species were higher than thresholds for detection of those calls. Our data provide the first opportunity to estimate distances over which specific communication signals may be effective (i.e. their ‘active space’) using masked thresholds for the signals themselves. Our results suggest that measures of peak sound pressure level, combined with the spectrum level of noise within the frequency channel having the greatest signal power relative to background noise, give the most similar results for estimating a signal's maximum communication distance across a variety of sounds. We provide a simple model for estimating likely detection and discrimination distances for the signals tested here. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.     

Stridulatory Sound-Production and Its Function in Females of the Cicada Subpsaltria yangi

Acoustic behavior plays a crucial role in many aspects of cicada biology, such as reproduction and intrasexual competition. Although female sound production has been reported in some cicada species, acoustic behavior of female cicadas has received little attention. In cicada Subpsaltria yangi, the females possess a pair of unusually well-developed stridulatory organs. Here, sound production and its function in females of this remarkable cicada species were investigated. We revealed that the females could produce sounds by stridulatory mechanism during pair formation, and the sounds were able to elicit both acoustic and phonotactic responses from males. In addition, the forewings would strike the body during performing stridulatory sound-producing movements, which generated impact sounds. Acoustic playback experiments indicated that the impact sounds played no role in the behavioral context of pair formation. This study provides the first experimental evidence that females of a cicada species can generate sounds by stridulatory mechanism. We anticipate that our results will promote acoustic studies on females of other cicada species which also possess stridulatory system.     

Social and vocal behavior in adult greater tube-nosed bats (Murina leucogaster)

Many studies have revealed the significant influence of the social nature and ecological niche of a species on the design and complexity of their communication sounds. The knowledge of communication sounds and particularly of the flexibility in their use among mammals, however, remains patchy. Being highly vocal and social, bats are well suited for investigating vocal plasticity as well as vocal diversity. Thus, the overall aim of this study was to test the presence of structural overlap between calls used in social communication and echolocation pulses emitted during foraging in greater tube-nosed bats (Murina leucogaster). Acoustic analysis and spectrotemporal decomposition of calls revealed a rich communication repertoire comprising 12 simple syllables and 5 composites with harmonics in the ultrasonic range. Simultaneous recording of vocal and social behavior in the same species yielded a strong correspondence between distinct behaviors and specific call types in support of Morton's motivation-structure hypothesis. Spectrographic analysis of call types also revealed the presence of modified components of echolocation pulses embedded within social calls. Altogether, the data suggest that bats can parse complex sounds into structurally simpler components that are recombined within behaviorally meaningful and multifunctional contexts.     

No pre-existing biases for heterospecific call traits in the frog Physalaemus enesefae

Previous phonotaxis studies with two species of the Physalaemuspustulosus species group indicated that female preferences for several heterospecific call traits resulted from sensory biases inherited from a common ancestor. In phonotaxis experiments, we determined whether Physalaemus enesefae, a distant relative of the P. pustulosus group, showed similar preferences for call traits not present in conspecific males. We presented females with a choice between the typical conspecific advertisement call and the same call to which we digitally appended a chuck from P. pustulosus, a squawk from P. freibergi, and an amplitude-modulated prefix from P. pustulatus. In addition we presented the advertisement call in doublets, a trait peculiar to P. coloradorum. We also analysed male vocal behaviour evoked in response to the same suite of stimuli. Physalaemus enesefae females did not prefer the calls of their own males with appended heterospecific traits over unmodified calls, nor conspecific calls in doublets over single calls. The lack of preference among females was not the result of a behavioural polymorphism. Female responses to repeated presentations of the same stimulus pair were not consistent. Males also did not show an enhanced vocal response to altered calls relative to the typical conspecific call. Consequently, there are no pre-existing biases for these heterospecific call traits in P. enesefae; pre-existing preferences in the P. pustulosus group could have been inherited from an ancestor not shared with P. enesefae, but data from other closely related species are needed to confirm this conclusion. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.