RESUMEN
Auditory streaming underlies a receiver's ability to organize complex mixtures of auditory input into distinct perceptual "streams" that represent different sound sources in the environment. During auditory streaming, sounds produced by the same source are integrated through time into a single, coherent auditory stream that is perceptually segregated from other concurrent sounds. Based on human psychoacoustic studies, one hypothesis regarding auditory streaming is that any sufficiently salient perceptual difference may lead to stream segregation. Here, we used the eastern grey treefrog, Hyla versicolor, to test this hypothesis in the context of vocal communication in a non-human animal. In this system, females choose their mate based on perceiving species-specific features of a male's pulsatile advertisement calls in social environments (choruses) characterized by mixtures of overlapping vocalizations. We employed an experimental paradigm from human psychoacoustics to design interleaved pulsatile sequences (ABAB ) that mimicked key features of the species' advertisement call, and in which alternating pulses differed in pulse rise time, which is a robust species recognition cue in eastern grey treefrogs. Using phonotaxis assays, we found no evidence that perceptually salient differences in pulse rise time promoted the segregation of interleaved pulse sequences into distinct auditory streams. These results do not support the hypothesis that any perceptually salient acoustic difference can be exploited as a cue for stream segregation in all species. We discuss these findings in the context of cues used for species recognition and auditory streaming.
RESUMEN
Selecting an attractive mate can involve trade-offs related to investment in sampling effort. Glucocorticoids like corticosterone (CORT) are involved in resolving energetic trade-offs. However, CORT is rarely studied in the context of mate choice, despite its elevated levels during reproductive readiness and the energetic transitions that characterize reproduction. Few systems are as well suited as anuran amphibians to evaluate how females resolve energetic trade-offs during mate choice. Phonotaxis tests provide a robust bioassay of mate choice that permit the precise measurement of inter-individual variation in traits such as choosiness-the willingness to pursue the most attractive mate despite costs. In Cope's gray treefrogs (Hyla chrysoscelis), females exhibit remarkable variation in circulating CORT as well as choosiness during mate choice, and a moderate dose of exogenous CORT rapidly (<1 h) and reliably induce large increases in choosiness. Here we measured the expression of glucocorticoid (GR) and mineralocorticoid (MR) receptors in the brains of females previously treated with exogenous CORT and tested for mate choosiness. We report a large decrease in GR expression in the hindbrain and midbrain of females that were treated with the moderate dosage of CORT-the same treatment group that exhibited a dramatic increase in choosiness following CORT treatment. This association, however, does not appear to be causal, as only forebrain GR levels, which are not affected by CORT injection, are positively associated with variation in choosiness. No strong effects were found for MR. We discuss these findings and suggest future studies to test the influence of glucocorticoids on mate choice.
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Anuros , Corticosterona , Animales , Femenino , Corticosterona/farmacología , Glucocorticoides , Encéfalo , ReproducciónRESUMEN
Albert Feng pioneered the study of neuroethology of sound localization in anurans by combining behavioral experiments on phonotaxis with detailed investigations of neural processing of sound direction from the periphery to the central nervous system. The main advantage of these studies is that many species of female frogs readily perform phonotaxis towards loudspeakers emitting the species-specific advertisement call. Behavioral studies using synthetic calls can identify which parameters are important for phonotaxis and also quantify localization accuracy. Feng was the first to investigate binaural processing using single-unit recordings in the first two auditory nuclei in the central auditory pathway and later investigated the directional properties of auditory nerve fibers with free-field stimulation. These studies showed not only that the frog ear is inherently directional by virtue of acoustical coupling or crosstalk between the two eardrums, but also confirmed that there are extratympanic pathways that affect directionality in the low-frequency region of the frog's hearing range. Feng's recordings in the midbrain also showed that directional information is enhanced by cross-midline inhibition. An important contribution toward the end of his career involved his participation in neuroethological research with a team of scientists working with frogs that produce ultrasonic calls.
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Localización de Sonidos , Femenino , Animales , Localización de Sonidos/fisiología , Audición/fisiología , Sonido , Vías Auditivas/fisiología , Anuros , Estimulación AcústicaRESUMEN
Amphibians have inner ears with two sensory papillae tuned to different frequency ranges of airborne sounds. In frogs, male advertisement calls possess distinct spectral components that match the tuning of one or both sensory papillae. Female preferences for the spectral content of advertisement calls can depend on signal amplitude and can vary among closely related lineages. In this study of Cope's gray tree frog (Hyla chrysoscelis), we investigated the amplitude dependence of female preferences for the spectral content of male advertisement calls, which have a "bimodal" spectrum with separate low-frequency (1.25 kHz) and high-frequency (2.5 kHz) components. In two-alternative choice tests, females generally preferred synthetic calls with bimodal spectra over "unimodal" calls having only one of the two spectral components. They also preferred unimodal calls with a high-frequency component over one with the low-frequency component. With few exceptions, preferences were largely independent of amplitude across both a 30 dB range of overall signal amplitude and an 11 dB range in the relative amplitudes of the two spectral components. We discuss these results in the context of evolutionary lability in female preferences for the spectral content of advertisement calls in North American tree frogs in the genus Hyla.
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Anuros , Vocalización Animal , Femenino , Animales , Estimulación Acústica , Vocalización Animal/fisiología , Anuros/fisiología , Sonido , Evolución BiológicaRESUMEN
Albert Feng was a pioneer in the field of auditory neuroethology who used frogs to investigate the neural basis of spectral and temporal processing and directional hearing. Among his many contributions was connecting neural mechanisms for sound pattern recognition and localization to the problems of auditory masking that frogs encounter when communicating in noisy, real-world environments. Feng's neurophysiological studies of auditory processing foreshadowed and inspired subsequent behavioral investigations of auditory masking in frogs. For frogs, vocal communication frequently occurs in breeding choruses, where males form dense aggregations and produce loud species-specific advertisement calls to attract potential mates and repel competitive rivals. In this review, we aim to highlight how Feng's research advanced our understanding of how frogs cope with noise. We structure our narrative around three themes woven throughout Feng's research-spectral, temporal, and directional processing-to illustrate how frogs can mitigate problems of auditory masking by exploiting frequency separation between signals and noise, temporal fluctuations in noise amplitude, and spatial separation between signals and noise. We conclude by proposing future research that would build on Feng's considerable legacy to advance our understanding of hearing and sound communication in frogs and other vertebrates.
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Ruido , Vocalización Animal , Masculino , Animales , Vocalización Animal/fisiología , Audición/fisiología , Percepción Auditiva/fisiología , Sonido , Anuros/fisiología , Enmascaramiento PerceptualRESUMEN
AbstractMany animals use signals to recognize familiar individuals but risk making mistakes because the signal properties of different individuals often overlap. Furthermore, outcomes of correct and incorrect decisions yield different fitness payoffs, and animals incur these payoffs at different frequencies depending on interaction rates. To understand how signal variation, payoffs, and interaction rates shape recognition decision rules, we studied male golden rocket frogs, which recognize the calls of territory neighbors and are less aggressive to neighbors than to strangers. We first quantified patterns of individual variation in call properties and predicted optimal discrimination thresholds using signal variation. We then measured thresholds for discriminating between neighbors and strangers using a habituation-discrimination field playback experiment. Territorial males discriminated between calls differing by 9%-12% in temporal properties, slightly higher than the predicted thresholds (5%-10%). Finally, we used a signal detection theory model to explore payoff and interaction rate parameters and found that the empirical threshold matched those predicted under ecologically realistic assumptions of infrequent encounters with strangers and relatively costly missed detections of strangers. We demonstrate that receivers group continuous variation in vocalizations into discrete social categories and that signal detection theory can be applied to understand evolved decision rules.
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Territorialidad , Vocalización Animal , Agresión , Animales , Anuros , Masculino , Reconocimiento en PsicologíaRESUMEN
Nearly 90% of flowering plants depend on animals for reproduction. One of the main rewards plants offer to pollinators for visitation is nectar. Nesocodon mauritianus (Campanulaceae) produces a blood-red nectar that has been proposed to serve as a visual attractant for pollinator visitation. Here, we show that the nectar's red color is derived from a previously undescribed alkaloid termed nesocodin. The first nectar produced is acidic and pale yellow in color, but slowly becomes alkaline before taking on its characteristic red color. Three enzymes secreted into the nectar are either necessary or sufficient for pigment production, including a carbonic anhydrase that increases nectar pH, an aryl-alcohol oxidase that produces a pigment precursor, and a ferritin-like catalase that protects the pigment from degradation by hydrogen peroxide. Our findings demonstrate how these three enzymatic activities allow for the condensation of sinapaldehyde and proline to form a pigment with a stable imine bond. We subsequently verified that synthetic nesocodin is indeed attractive to Phelsuma geckos, the most likely pollinators of Nesocodon We also identify nesocodin in the red nectar of the distantly related and hummingbird-visited Jaltomata herrerae and provide molecular evidence for convergent evolution of this trait. This work cumulatively identifies a convergently evolved trait in two vertebrate-pollinated species, suggesting that the red pigment is selectively favored and that only a limited number of compounds are likely to underlie this type of adaptation.
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Flores/metabolismo , Magnoliopsida/metabolismo , Pigmentación/fisiología , Néctar de las Plantas/metabolismo , Polen/metabolismo , Adaptación Fisiológica/fisiología , Animales , Aves/fisiología , Lagartos/fisiología , Polinización/fisiología , Reproducción/fisiologíaRESUMEN
Animals recognize familiar individuals to perform a variety of important social behaviors. Social recognition is often mediated by communication between signalers who produce signals that contain identity information and receivers who categorize these signals based on previous experience. We tested two hypotheses about adaptations in signalers and receivers that enable the evolution of social recognition using two species of closely related territorial poison frogs. Male golden rocket frogs (Anomaloglossus beebei) recognize the advertisement calls of conspecific territory neighbors and display a "dear enemy effect" by responding less aggressively to neighbors than strangers, whereas male Kai rocket frogs (Anomaloglossus kaiei) do not. Our results did not support the identity signaling hypothesis: both species produced advertisement calls that contain similar amounts of identity information. Our results did support the identity reception hypothesis: both species exhibited habituation of aggression to playbacks simulating the arrival of a new neighbor, but only golden rocket frogs showed renewed aggression when they subsequently heard calls from a different male. These results suggest that an ancestral mechanism of plasticity in aggression common among frogs has been modified through natural selection to be specific to calls of individual males in golden rocket frogs, enabling a social recognition system.
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Anuros , Territorialidad , Agresión , Animales , Anuros/genética , Humanos , Masculino , Reconocimiento en Psicología , Conducta Social , Vocalización AnimalRESUMEN
Sexual traits that promote species recognition are important drivers of reproductive isolation, especially among closely related species. Identifying neural processes that shape species differences in recognition is crucial for understanding the causal mechanisms of reproductive isolation. Temporal patterns are salient features of sexual signals that are widely used in species recognition by several taxa, including anurans. Recent advances in our understanding of temporal processing by the anuran auditory system provide an opportunity to investigate the neural basis of species-specific recognition. The anuran inferior colliculus consists of neurons that are selective for temporal features of calls. Of potential relevance are auditory neurons known as interval-counting neurons (ICNs) that are often selective for the pulse rate of conspecific advertisement calls. Here, we tested the hypothesis that ICNs mediate acoustic species recognition by exploiting the known differences in temporal selectivity in two cryptic species of gray treefrog (Hyla chrysoscelis and Hyla versicolor). We examined the extent to which the threshold number of pulses required to elicit behavioral responses from females and neural responses from ICNs was similar within each species but potentially different between the two species. In support of our hypothesis, we found that a species difference in behavioral pulse number thresholds closely matched the species difference in neural pulse number thresholds. However, this relationship held only for ICNs that exhibited band-pass tuning for conspecific pulse rates. Together, these findings suggest that differences in temporal processing of a subset of ICNs provide a mechanistic explanation for reproductive isolation between two cryptic treefrog species.
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Colículos Inferiores , Vocalización Animal , Estimulación Acústica , Acústica , Animales , Anuros , Percepción Auditiva , FemeninoRESUMEN
Most animals experience reproductive transitions in their lives; for example, reaching reproductive maturity or cycling in and out of breeding condition. Some reproductive transitions are abrupt, while others are more gradual. In most cases, changes in communication between the sexes follow the time course of these reproductive transitions and are typically thought to be coordinated by steroid hormones. We know a great deal about hormonal control of communication behaviors in birds and frogs, as well as the central neural control of these behaviors. There has also been significant interest in the effects of steroid hormones on central nervous system structures that control both the production and reception of communication signals associated with reproductive behaviors. However, peripheral sensory structures have typically received less attention, although there has been growing interest in recent years. It is becoming clear that peripheral sensory systems play an important role in reproductive communication, are plastic across reproductive conditions, and, in some cases, this plasticity may be mediated by steroid hormones. In this article, we discuss recent evidence for the role of peripheral auditory structures in reproductive communication in birds and frogs, the plasticity of the peripheral auditory system, and the role of steroid hormones in mediating the effects of the peripheral auditory system on reproductive communication. We focus on both seasonal and acute reproductive transitions, introduce new data on the role of hormones in modulating seasonal patterns, and make recommendations for future work.
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Anuros/fisiología , Hormonas/fisiología , Reproducción , Pájaros Cantores , Vocalización Animal , Animales , Conducta Sexual Animal , Pájaros Cantores/fisiologíaRESUMEN
The genus Raorchestes is a large radiation of Old World tree frogs for which the Western Ghats in Peninsular India is the major center for origin and diversification. Extensive studies on this group during the past two decades have resolved long-standing taxonomic confusions and uncovered several new species, resulting in a four-fold increase in the number of known Raorchestes frogs from this region. Our ongoing research has revealed another five new species in the genus, formally described as Raorchestes drutaahu sp. nov., Raorchestes kakkayamensis sp. nov., Raorchestes keirasabinae sp. nov., Raorchestes sanjappai sp. nov., and Raorchestes vellikkannan sp. nov., all from the State of Kerala in southern Western Ghats. Based on new collections, we also provide insights on the taxonomic identity of three previously known taxa. Furthermore, since attempts for an up-to-date comprehensive study of this taxonomically challenging genus using multiple integrative taxonomic approaches have been lacking, here we review the systematic affinities of all known Raorchestes species and define 16 species groups based on evidence from multi-gene (2,327 bp) phylogenetic analyses, several morphological characters (including eye colouration and pattern), and acoustic parameters (temporal and spectral properties, as well as calling height). The results of our study present novel insights to facilitate a better working taxonomy for this rather speciose and morphologically conserved radiation of shrub frogs. This will further enable proper field identification, provide momentum for multi-disciplinary studies, as well as assist conservation of one of the most colourful and acoustically diverse frog groups of the Western Ghats biodiversity hotspot.
RESUMEN
Environmental noise is a major source of selection on animal sensory and communication systems. The acoustic signals of other animals represent particularly potent sources of noise for chorusing insects, frogs, and birds, which contend with a multi-species analog of the human "cocktail party problem" (i.e., our difficulty following speech in crowds). However, current knowledge of the diverse adaptations that function to solve noise problems in nonhuman animals remains limited. Here, we show that a lung-to-ear sound transmission pathway in frogs serves a heretofore unknown noise-control function in vertebrate hearing and sound communication. Inflated lungs improve the signal-to-noise ratio for communication by enhancing the spectral contrast in received vocalizations in ways analogous to signal processing algorithms used in hearing aids and cochlear implants. Laser vibrometry revealed that the resonance of inflated lungs selectively reduces the tympanum's sensitivity to frequencies between the two spectral peaks present in conspecific mating calls. Social network analysis of continent-scale citizen science data on frog calling behavior revealed that the calls of other frog species in multi-species choruses can be a prominent source of environmental noise attenuated by the lungs. Physiological modeling of peripheral frequency tuning indicated that inflated lungs could reduce both auditory masking and suppression of neural responses to mating calls by environmental noise. Together, these data suggest an ancient adaptation for detecting sound via the lungs has been evolutionarily co-opted to create auditory contrast enhancement that contributes to solving a multi-species cocktail party problem.
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Comunicación Animal , Anuros/fisiología , Audición , Ruido , Animales , Pulmón/fisiología , Relación Señal-RuidoRESUMEN
Glucocorticoids (GCs) are rarely studied in the context of female mate choice, despite the expression of receptors for these products in sexual, sensory and decision-making brain areas. Here we investigated the effects of GC concentrations on three aspects of female sexual behavior in breeding Cope's gray treefrogs (Hyla chrysoscelis): proceptivity-a measure of sexual motivation, intraspecific mate preferences, and mate choosiness. To our knowledge this is the first experimental study on the endocrine basis of mate choosiness. We predicted that mate choosiness-forfeiting an initial mate preference to pursue a suddenly more attractive mate-would be particularly impacted by elevated GCs with moderate GC levels associated with greater choosiness. We found support for this predicted inverted-U relationship. Females in the control group (no injection) showed no change in choosiness across timepoints. In contrast, females in the vehicle, Low (20 ng g-1) and High (180 ng g-1) corticosterone groups exhibited a nominal decline in choosiness after injection, suggesting that the experience of injection has little or perhaps slightly suppressive effects on female choosiness. Females in the moderate dose group (60 ng g-1), however, exhibited a significant increase (>100%) in choosiness. Further, we found no effect of elevated GCs on sexual proceptivity or the species-typical preference for longer calls. These findings may reflect a buffering of primary sensory areas in the brain against elevated GCs. The recruitment of other cognitive processes during active decision-making, however, may facilitate GC modulation of mate choosiness, thereby promoting tactical plasticity at this critical life history juncture.
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Glucocorticoides , Preferencia en el Apareamiento Animal , Animales , Anuros , Femenino , Reproducción , Conducta Sexual AnimalRESUMEN
For many animals, navigating their environment requires an ability to organize continuous streams of sensory input into discrete 'perceptual objects' that correspond to physical entities in visual and auditory scenes. The human visual and auditory systems follow several Gestalt laws of perceptual organization to bind constituent features into coherent perceptual objects. A largely unexplored question is whether nonhuman animals follow similar Gestalt laws in perceiving behaviourally relevant stimuli, such as communication signals. We used females of Cope's grey treefrog (Hyla chrysoscelis) to test the hypothesis that temporal coherence-a powerful Gestalt principle in human auditory scene analysis-promotes perceptual binding in forming auditory objects of species-typical vocalizations. According to the principle of temporal coherence, sound elements that start and stop at the same time or that modulate coherently over time are likely to become bound together into the same auditory object. We found that the natural temporal coherence between two spectral components of advertisement calls promotes their perceptual binding into auditory objects of advertisement calls. Our findings confirm the broad ecological validity of temporal coherence as a Gestalt law of auditory perceptual organization guiding the formation of biologically relevant perceptual objects in animal behaviour.
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Anuros , Vocalización Animal , Estimulación Acústica , Animales , Percepción Auditiva , Conducta Animal , Comunicación , Femenino , Humanos , SonidoRESUMEN
Amphibians are unique among extant vertebrates in having middle ear cavities that are internally coupled to each other and to the lungs. In frogs, the lung-to-ear sound transmission pathway can influence the tympanum's inherent directionality, but what role such effects might play in directional hearing remains unclear. In this study of the American green treefrog (Hyla cinerea), we tested the hypothesis that the lung-to-ear sound transmission pathway functions to improve directional hearing, particularly in the context of intraspecific sexual communication. Using laser vibrometry, we measured the tympanum's vibration amplitude in females in response to a frequency modulated sweep presented from 12 sound incidence angles in azimuth. Tympanum directionality was determined across three states of lung inflation (inflated, deflated, reinflated) both for a single tympanum in the form of the vibration amplitude difference (VAD) and for binaural comparisons in the form of the interaural vibration amplitude difference (IVAD). The state of lung inflation had negligible effects (typically less than 0.5â dB) on both VADs and IVADs at frequencies emphasized in the advertisement calls produced by conspecific males (834 and 2730â Hz). Directionality at the peak resonance frequency of the lungs (1558â Hz) was improved by â¼3â dB for a single tympanum when the lungs were inflated versus deflated, but IVADs were not impacted by the state of lung inflation. Based on these results, we reject the hypothesis that the lung-to-ear sound transmission pathway functions to improve directional hearing in frogs.
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Localización de Sonidos , Estimulación Acústica , Animales , Anuros , Femenino , Audición , Pulmón , Masculino , SonidoRESUMEN
Like political stump speeches and product advertisements, animal signals are highly repetitive and function to persuade receivers to adopt behaviors benefiting the signaler. And like potential constituents and consumers, receivers assess signals to inform their behavioral decisions. However, inconsistency in sexual signals is widespread and potentially injects uncertainty into mating decisions. Here, we show that females fail to make optimal mating decisions based on assessments of signal quality due to inconsistency in signal production. Natural levels of inconsistency markedly reduced female preference expression for a nonarbitrary signal of male quality. Inconsistency reshaped preferences even more profoundly than the better-known impediment of ambient noise. To our knowledge, this is the first demonstration of how inconsistent messaging degrades optimal decision-making in animals, with implications for understanding signal evolution.
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Preferencia en el Apareamiento Animal , Animales , Comunicación Celular , Femenino , Masculino , Reproducción , Conducta Sexual Animal , Transducción de SeñalRESUMEN
Accurately quantifying animal activity and movements is of fundamental importance in a broad range of disciplines, from biomedical research to behavioral ecology. In many instances, it is desirable to measure natural movements in controlled sensory environments in which the animals are not physically or chemically restrained, but their movements are nevertheless constrained to occur within a fixed volume. Here, we describe a novel device to quantify the movements of small animals in response to sensory stimulation. The device consists of an Arduino controlled inertial measurement unit that senses angular velocity (along three axes) of a suspended mesh enclosure that temporarily houses the animal subject. We validated the device by measuring the phonotaxis behavior of gravid female frogs in response to acoustic broadcasts of male mating calls. The system, as designed, proved effective at measuring natural movements made in response to acoustic stimulation.
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Both behavioral receptivity and neural sensitivity to acoustic mate attraction signals vary across the reproductive cycle, particularly in seasonally breeding animals. Across a variety of taxa receptivity to signals increases, as does peripheral auditory sensitivity, as females transition from a non-breeding to breeding condition. We recently documented decreases in receptivity to acoustic mate attraction signals and circulating hormone levels, but an increase in peripheral auditory sensitivity to call-like stimuli following oviposition in Cope's gray treefrogs (Hyla chrysoscelis). However, it is not known if changes in auditory sensitivity are confined to the frequency range of calls, or if they result from more generalized changes in the auditory periphery. Here, we used auditory brainstem responses (ABRs) to evaluate peripheral frequency sensitivity in female Cope's gray treefrogs before and after oviposition. We found lower ABR thresholds, greater ABR amplitudes, and shorter ABR latencies following oviposition. Changes were most pronounced and consistent at lower frequencies associated with the amphibian papilla, but were also detectable at higher frequencies corresponding to the tuning of the basilar papilla. Furthermore, only ABR latencies were correlated with circulating steroid hormones (testosterone). Changes in peripheral processing may result from changes in metabolic function or sensorineural adaptation to chorus noise.
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Anuros/fisiología , Umbral Auditivo/fisiología , Oviposición/fisiología , Animales , Potenciales Evocados Auditivos del Tronco Encefálico/fisiología , FemeninoRESUMEN
In seasonal breeders, there are behavioral, endocrine, and neural adaptations that promote the sexual receptivity of females and tune their sensory systems to detect and discriminate among advertising males and to successfully copulate. What happens immediately after this key life history event is unclear, but this transitional moment offers a window into the mechanisms that remodel sexual phenotypes. In this study of wild female Cope's gray treefrogs (Hyla chrysoscelis), we tested the hypothesis that oviposition results in a suite of coordinated changes in the sexual phenotype. Specifically, we predicted that sexual receptivity and discrimination behaviors would decline along with circulating concentrations of steroid hormones (corticosterone, estradiol, testosterone) and auditory sensitivity to the acoustic frequencies emphasized in male advertisement calls. We conducted these trait measurements before and after oviposition (ca. 24-h period). There was a 100% decrease in behavioral responsiveness after oviposition, and the concentrations of all three steroids plummeted during this brief window of time, especially testosterone. Moreover, higher concentrations of corticosterone-an important component of the endocrine stress response-were associated with longer response latencies, suggesting that adrenal hormones should be considered in future studies on the hormonal basis of mate choice. Counter to our prediction, auditory sensitivity increased following oviposition, and the amplitude of the auditory brainstem response was influenced by concentrations of estradiol. In pre-oviposition females auditory sensitivity diminished with increasing estradiol concentrations, while sensitivity increased with increasing estradiol concentrations in post-oviposition females, suggesting non-linear estrogenic modulation of peripheral auditory neural recruitment. Overall, our results indicate that there is considerable remodeling of behavioral output following oviposition that co-occurs with changes in both endocrine and sensory physiology.