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Although mate searching behavior in female túngara frogs (Physalaemus pustulosus) is nocturnal and largely mediated by acoustic cues, male signaling includes visual cues produced by the vocal sac. To compensate for these low light conditions, visual sensitivity in females is modulated when they are in a reproductive state, as retinal thresholds are decreased. This study tested whether estradiol (E2) plays a role in this modulation. Female túngara frogs were injected with either human chorionic gonadotropin (hCG) or a combination of hCG and fadrozole. hCG induces a reproductive state and increases retinal sensitivity, while fadrozole is an aromatase inhibitor that blocks hCG-induced E2 synthesis. In an analysis of scotopic electroretinograms (ERGs), hCG treatment lowered the threshold for eliciting a b-wave response, whereas the addition of fadrozole abolished this effect, matching thresholds in non-reproductive saline-injected controls. This suggests that blocking E2 synthesis blocked the hCG-mediated reproductive modulation of retinal sensitivity. By implicating E2 in control of retinal sensitivity, our data add to growing evidence that the targets of gonadal steroid feedback loops include sensory receptor organs, where stimulus sensitivity may be modulated, rather than more central brain nuclei, where modulation may affect mechanisms involved in motivation., (© The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.)

Noise is a common problem in animal communication. We know little, however, about how animals communicate in the presence of noise using multimodal signals. Multimodal signals are hypothesised to be favoured by evolution because they increase the efficacy of detection and discrimination in noisy environments. We tested the hypothesis that female túngara frogs' responses to attractive male advertisement calls are improved in noise when a visual signal component is added to the available choices. We tested this at two levels of decision complexity (two and three choices). In a two-choice test, the presence of noise did not reduce female preferences for attractive calls. The visual component of a calling male, associated with an unattractive call, also did not reduce preference for attractive calls in the absence of noise. In the presence of noise, however, females were more likely to choose an unattractive call coupled with the visual component. In three-choice tests, the presence of noise alone reduced female responses to attractive calls and this was not strongly affected by the presence or absence of visual components. The responses in these experiments fail to support the multimodal signal efficacy hypothesis. Instead, the data suggest that audio-visual perception and cognitive processing, related to mate choice decisions, are dependent on the complexity of the sensory scene., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)

Animals choosing particular display sites often balance sexual and natural selection pressures. Here we assess how physical properties of display sites can alter this balance by influencing signal production and attractiveness of the túngara frog (Physalaemus pustulosus). Males that call from very shallow water bodies (few mm depth) benefit from reduced predation risk, but by manipulating water levels, we show that this comes at a cost of reduced attractiveness to females. Our data show that calling from shallower water reduces a male's ability to float, limits the inflation of his vocal sac, and consequently reduces signal conspicuousness in terms of amplitude and complexity. Our results demonstrate that display site properties can set limits on signal production and attractiveness and may hence influence signal evolution. Signallers may shift between sites or engineer their display location, which can play a crucial role in signal divergence and speciation, particularly in a rapidly changing world.

Multimodal signaling is common in communication systems. Depending on the species, individual signal components may be produced synchronously as a result of physiological constraint (fixed) or each component may be produced independently (fluid) in time. For animals that rely on fixed signals, a basic prediction is that asynchrony between the components should degrade the perception of signal salience, reducing receiver response. Male túngara frogs, Physalaemus pustulosus, produce a fixed multisensory courtship signal by vocalizing with two call components (whines and chucks) and inflating a vocal sac (visual component). Using a robotic frog, we tested female responses to variation in the temporal arrangement between acoustic and visual components. When the visual component lagged a complex call (whine + chuck), females largely rejected this asynchronous multisensory signal in favor of the complex call absent the visual cue. When the chuck component was removed from one call, but the robofrog inflation lagged the complex call, females responded strongly to the asynchronous multimodal signal. When the chuck component was removed from both calls, females reversed preference and responded positively to the asynchronous multisensory signal. When the visual component preceded the call, females responded as often to the multimodal signal as to the call alone. These data show that asynchrony of a normally fixed signal does reduce receiver responsiveness. The magnitude and overall response, however, depend on specific temporal interactions between the acoustic and visual components. The sensitivity of túngara frogs to lagging visual cues, but not leading ones, and the influence of acoustic signal content on the perception of visual asynchrony is similar to those reported in human psychophysics literature. Virtually all acoustically communicating animals must conduct auditory scene analyses and identify the source of signals. Our data suggest that some basic audiovisual neural integration processes may be at work in the vertebrate brain., (Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology 2017. This work is written by US Government employees and is in the public domain in the US.)

Pathogen-driven selection can favour major histocompatibility complex (MHC) alleles that confer immunological resistance to specific diseases. However, strong directional selection should deplete genetic variation necessary for robust immune function in the absence of balancing selection or challenges presented by other pathogens. We examined selection dynamics at one MHC class II (MHC-II) locus across Panamanian populations of the túngara frog, Physalaemus pustulosus, infected by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). We compared MHC-II diversity in highland túngara frog populations, where amphibian communities have experienced declines owing to Bd, with those in the lowland region that have shown no evidence of decline. Highland region frogs had MHC variants that confer resistance to Bd. Variant fixation appeared to occur by directional selection rather than inbreeding, as overall genetic variation persisted in populations. In Bd-infected lowland sites, however, selective advantage may accrue to individuals with only one Bd-resistance allele, which were more frequent. Environmental conditions in lowlands should be less favourable for Bd infection, which may reduce selection for specific Bd resistance in hosts. Our results suggest that MHC selection dynamics fluctuate in túngara frog populations as a function of the favourability of habitat to pathogen spread and the vulnerability of hosts to infection., (© 2016 The Author(s).)

Chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), is an emergent infectious disease partially responsible for worldwide amphibian population declines. The spread of Bd along highland habitats (> 500 meters above sea level, m a.s.l.) of Costa Rica and Panamá is well documented and has been linked to amphibian population collapses. In contrast, data are scarce on the prevalence and dispersal of Bd in lowland habitats where amphibians may be infected but asymptomatic. Here we describe the spread (2009 to 2014) of Bd across lowland habitats east of the Panamá Canal (< 500 m a.s.l.) with a focus on the Túngara frog (Physalaemus [Engystomops] pustulosus), one of the most common and abundant frog species in this region. Highland populations in western Panamá were already infected with Bd at the start of the study, which was consistent with previous studies indicating that Bd is enzootic in this region. In central Panamá, we collected the first positive samples in 2010, and by 2014, we detected Bd from remote sites in eastern Panamá (Darién National Park). We discuss the importance of studying Bd in lowland species, which may serve as potential reservoirs and agents of dispersal of Bd to highland species that are more susceptible to chytridiomycosis.

Many sexual displays contain multiple components that are received through a variety of sensory modalities. Primary and secondary signal components can interact to induce novel receiver responses and become targets of sexual selection as complex signals. However, predators can also use these complex signals for prey assessment, which may limit the evolution of elaborate sexual signals. We tested whether a multimodal sexual display of the male túngara frog (Physalaemus pustulosus) increases predation risk from the fringe-lipped bat (Trachops cirrhosus) when compared with a unimodal display. We gave bats a choice to attack one of two frog models: a model with a vocal sac moving in synchrony with a mating call (multisensory cue), or a control model with the call but no vocal sac movement (unimodal cue). Bats preferred to attack the model associated with the multimodal display. Furthermore, we determined that bats perceive the vocal sac using echolocation rather than visual cues. Our data illustrate the costs associated with multimodal signaling and that sexual and natural selection pressures on the same trait are not always mediated through the same sensory modalities. These data are important when considering the role of environmental fluctuations on signal evolution as different sensory modalities will be differentially affected., (© 2014. Published by The Company of Biologists Ltd.)

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for 'more musical' sounds., (© 2014 The Author(s) Published by the Royal Society. All rights reserved.)

Animals have multiple senses through which they detect their surroundings and often integrate sensory information across different modalities to generate perceptions. Animal communication, likewise, often consists of signals containing stimuli processed by different senses. Stimuli with different physical forms (i.e., from different sensory modalities) travel at different speeds. As a consequence, multimodal stimuli simultaneously emitted at a source can arrive at a receiver at different times. Such differences in arrival time can provide unique information about the distance to the source. Male túngara frogs (Physalaemus pustulosus) call from ponds to attract females and to repel males. Production of the sound incidentally creates ripples on the water surface, providing a multimodal cue. We tested whether male frogs attend to distance-dependent cues created by a calling rival and whether their response depends on crossmodal comparisons. In a first experiment, we showed distance-dependent changes in vocal behavior: males responded more strongly with decreasing distance to a mimicked rival. In a second experiment, we showed that males can discriminate between relatively near and far rivals by using a combination of unimodal cues, specifically amplitude changes of sound and water waves, as well as crossmodal differences in arrival time. Our data reveal that animals can compare the arrival time of simultaneously emitted multimodal cues to obtain information on relative distance to a source. We speculate that communicative benefits from crossmodal comparison may have been an important driver of the evolution of elaborate multimodal displays., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

Air-driven vocal production systems such as those found in mammals, birds, and anurans (frogs and toads) combine pneumatic and mechanical elements in species-specific ways to produce a diversity of communication signals. This study uses bond graphs to model a generalized anuran vocal production system. Bond graphs allow an incremental approach to modeling dynamic physical systems involving different domains. Anurans provide an example of how signal diversity results from variation in the structure and behavior of vocal system elements. This paper first proposes a bond graph model of the integrated anuran vocal system as a framework for future study. It then presents a simulated submodel of the anuran sound source that produces sustained oscillations in vocal fold displacement and air flow through the larynx. The modeling approach illustrated here should prove of general applicability to other biological sound production systems, and will allow researchers to study the biomechanics of vocal production as well as the functional congruence and evolution of groups of traits within integrated vocal systems.

Most studies addressing the development of animal communication have focused on signal production rather than receiver decoding, and similar emphasis has been given to learning over nonlearning. But receivers are an integral part of a communication network, and nonlearned mechanisms appear to be more ubiquitous than learned ones in the communication systems of most animals. Here we review the results of recent experiments and outline future directions for integrative studies on the development of a primarily nonlearned behaviour-recognition of communication signals during ontogeny in a tropical frog. The results suggest that antecedents to adult behaviours might be a common feature of developing organisms. Given the essential role that acoustic communication serves in reproduction for many organisms and that receivers can exert strong influence on the evolution of signals, understanding the evolutionary developmental basis of mate recognition will provide new insights into the evolution of communication systems.

The main premise of this article is that various cognitive functions involved in signal analysis, memory, and decision making, all modulated by the animal's internal milieu, can generate selection for the forms of signals used in social interactions. Thus, just as an animal's view of its world, its Umwelt, determines how it interacts with its ecological niche, it can influence the evolution of its social niche. Thus, the brain is not only a landscape on which selection can act, but also it is a powerful source of selection on the animal's social niche., (© The Author 2011. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.)

Psychophysics measures the relationship between a stimulus's physical magnitude and its perceived magnitude. Because decisions are based on perception of stimuli, this relationship is critical to understanding decision-making. We tested whether psychophysical laws explain how female túngara frogs (Physalaemus pustulosus) and frog-eating bats (Trachops cirrhosus) compare male frog calls, and how this imposes selection on call evolution. Although both frogs and bats prefer more elaborate calls, they are less selective as call elaboration increases, because preference is based on stimulus ratios. Thus, as call elaboration increases, both relative attractiveness and relative predation risk decrease because of how receivers perceive and compare stimuli. Our data show that female cognition can limit the evolution of sexual signal elaboration.

Multimodal signals (acoustic+visual) are known to be used by many anuran amphibians during courtship displays. The relative degree to which each signal component influences female mate choice, however, remains poorly understood. In this study we used a robotic frog with an inflating vocal sac and acoustic playbacks to document responses of female túngara frogs to unimodal signal components (acoustic and visual). We then tested female responses to a synchronous multimodal signal. Finally, we tested the influence of spatial and temporal variation between signal components for female attraction. Females failed to approach the isolated visual cue of the robotic frog and they showed a significant preference for the call over the spatially separate robotic frog. When presented with a call that was temporally synchronous with the vocal sac inflation of the robotic frog, females did not show a significant preference for this over the call alone; when presented with a call that was temporally asynchronous with vocal sac inflation of the robotic frog, females discriminated strongly against the asynchronous multimodal signal in favor of the call alone. Our data suggest that although the visual cue is neither necessary nor sufficient for attraction, it can strongly modulate mate choice if females perceive a temporal disjunction relative to the primary acoustic signal.

Males and females can differ both in the social behaviors they perform and in the contexts in which they engage in these behaviors. One possible mechanism of sex differences in behavior is a sexual dimorphism in the relay of sensory information to motor areas, but no studies have examined the role of such a relay in vertebrate sexually dimorphic behaviors. We used egr-1 expression as a marker of neural activation in frogs exposed to conspecific and heterospecific acoustic signals to compare activation patterns throughout the brains of males and females. We determined how the sexes differ in the transformation of social signals into motor responses in the context of social communication. We examined the relationships between egr-1 mRNA levels in the auditory midbrain and forebrain areas, as well as how forebrain expression related to the behavioral responses of the animals. Forebrain network activation patterns and forebrain-behavior relationships were similar in males and females. By contrast, we found a sex difference in the relationship between midbrain and forebrain activation; midbrain auditory responses predicted forebrain responses in females but not in males. This sex difference suggests that sensory inputs differentially regulate motor systems underlying social behaviors in males and females. This sensorimotor transformation may be a common locus for generating sex differences in behavior.

Background: Uncovering how populations of a species differ genetically and ecologically is important for understanding evolutionary processes. Here we combine population genetic methods (microsatellites) with phylogenetic information (mtDNA) to define genetic population clusters of the wide-spread Neotropical túngara frog (Physalaemus pustulosus). We measure gene flow and migration within and between population clusters and compare genetic diversity between population clusters. By applying ecological niche modeling we determine whether the two most divergent genetic groups of the túngara frog (1) inhabit different habitats, and (2) are separated geographically by unsuitable habitat across a gap in the distribution., Results: Most population structure is captured by dividing all sample localities into two allopatric genetic lineages. The Northern genetic lineage (NW Costa Rica) is genetically homogenous while the Southern lineage (SW Costa Rica and Panama) is sub-divided into three population clusters by both microsatellite and mtDNA analyses. Gene flow is higher within the Northern lineage than within the Southern lineage, perhaps due to increased landscape heterogeneity in the South. Niche modeling reveals differences in suitable habitat between the Northern and Southern lineages: the Northern lineage inhabits dry/pine-oak forests, while the Southern lineage is confined to tropical moist forests. Both lineages seem to have had little movement across the distribution gap, which persisted during the last glacial maximum. The lack of movement was more pronounced for the Southern lineage than for the Northern lineage., Conclusions: This study confirms the finding of previous studies that túngara frogs diverged into two allopatric genetic lineages north and south of the gap in the distribution in central Costa Rica several million years ago. The allopatric distribution is attributed to unsuitable habitat and probably other unknown ecological factors present across the distribution gap. Niche conservatism possibly contributes to preventing movements across the gap and gene flow between both groups. Genetic and ecological data indicate that there is the potential for ecological divergence in allopatry between lineages. In this context we discuss whether the Northern and Southern lineages should be recognized as separate species, and we conclude that further studies of pre- and post-zygotic isolation are needed for a final assessment. Identified population clusters should motivate future behavioral and ecological research regarding within-species biodiversity and speciation mechanisms.

A new study shows that biparental care in frogs is more likely to evolve when tadpoles are reared under environmentally harsh conditions. Biparental care facilitates both social monogamy and genetic monogamy; frogs that work together to raise their offspring have higher mating fidelity to one another., ((c) 2010 Elsevier Ltd. All rights reserved.)

Females often prefer to mate with males who produce complex signals. It is not clear why they do so. Females might prefer complexity if it predicts mate quality, or signals might evolve complexity to exploit females' sensory or cognitive biases. We tested whether complexity increases active time, the period over which a signal influences a receiver's response to that signal. Mating signals are often ephemeral, yet their active time has largely been ignored. Here we demonstrate that signal complexity influences active time in túngara frogs. Male advertisement calls consist of frequency sweeps (whines) followed by 0-7 high-frequency bursts (chucks). Females preferentially approach complex (whines with chucks) over simple (whines alone) calls but do not consistently prefer greater complexity, so the function of multiple chucks has been uncertain. We found that females remember which speaker previously broadcast complex calls when choosing between simple calls broadcast after a delay. This effect occurred for calls with multiple chucks, but not with single chucks. Neither motivation nor orientation behavior differed with chuck number, suggesting that results are due to differential memory. Thus, female memory could favor the evolution of increasing signal complexity through sexual selection., (2010 Elsevier Ltd. All rights reserved.)

In order for a signal to be transmitted from a sender to a receiver, the receiver must be within the active space of the signal. If patterns of sound radiation are not omnidirectional, the position as well as the distance of the receiver relative to the sender is critical. In previous measurements of the horizontal directivity of mating calls of frogs, the signals were analyzed using peak or root-mean-square analysis and resulted in broadband directivities that ranged from negligible to a maximum of approximately 5 dB. Idealized laboratory measurements of the patterns of acoustic radiation of the mating calls of male tungara frogs (Physalaemus pustulosus), along axes relevant to three receivers in this communication network, female frogs in the horizontal plane, and frog-eating bats and blood-sucking flies above the ground, are reported. The highest sound pressure level was radiated directly above the frog, with a 6 dB reduction radiated along the horizontal direction. Band-limited directivities were significantly greater than broadband directivities, with a maximum directivity of 20 dB in the vertical plane for harmonics near 6 kHz. The implications with regard to mating and predator-prey interactions are discussed.

In many mating systems, both sexes respond to the same sexual signal. In frogs, males typically call in response to advertisement calls, while females approach male calls in choosing a mate. The costs of signal detection errors are expected to differ between the sexes. Missed opportunities are costly for males because ignoring a signal results in failing to compete with rivals for mates, while their cost for misidentification is lower (time and energy displaying to the incorrect target). By contrast, for females, the cost of misidentification is high (mating with incorrect species or low-quality partner), while their cost for missed opportunity is lower because the operational sex ratio puts females at a premium. Consequently, females should be more selective in their response to signal variation than males. We report that presumed sexual differences in selectivity in túngara frogs (Physalaemus pustulosus) are task-specific rather than sex-specific. As predicted, male túngara frogs are less selective in their vocal responses than are females in their phonotactic responses. Males exhibiting phonotaxis to the same calls, however, are as selective as females, and are significantly more selective than when they respond vocally to the same calls. Our study shows that apparent differences between the sexes emerge from differences in the behaviours themselves and are not intrinsic to each sex. Analogous behavioural differences might confound sex differences in other systems; thus, we suggest consideration of the behavioural plasticity of sex as well as its stereotypy.

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.

The vocal sac is a visually conspicuous attribute of most male frogs, but its role in visual communication has only been demonstrated recently in diurnally displaying frogs. Here we characterized the spectral properties of the inflated vocal sac of male túngara frogs (Physalaemus pustulosus), a nocturnal species, and túngara visual sensitivity to this cue across reproductive state and sex. We measured the spectral and total reflectance of different male body regions, including inflated and non-inflated vocal sacs, along with samples of the visual background against which males are perceived. Inflated vocal sacs were the most reflective of all body parts, being one log unit more reflective than background materials. We utilized an optomotor drum with black stripes and stripes that mimicked the spectral reflectance of the inflated vocal sacs with various nocturnal light intensities to measure the visual sensitivity thresholds of males, non-reproductive females and reproductive females. All three groups exhibited visual sensitivities corresponding to intensities below moonless conditions in open habitats or at the edge of secondary tropical forests. Reproductive females exhibited the greatest visual sensitivity of all groups, and were significantly more sensitive than non-reproductive females. Though the mechanism for this physiological difference between reproductive and non-reproductive females is unknown, it is consistent with previously observed patterns of light-dependent phonotaxic behavior in túngaras. We suggest that the visual ecology of the vocal sac, especially in nocturnal frogs, offers a rich source for investigations of visual ecology and physiological regulation of vision.

Interactions with heterospecifics can promote the evolution of divergent mating behaviours between populations that do and do not occur with heterospecifics. This process--reproductive character displacement--potentially results from selection to minimize the risk of mating with heterospecifics. We sought to determine whether heterospecific interactions lead to divergence of female preferences for aspects of conspecific male signals. We used artificial neural network models to simulate a mate recognition system in which females co-occur with different heterospecifics in different populations. Populations that evolved conspecific recognition in the presence of different heterospecifics varied in their preferences for aspects of conspecific male signals. When we tested networks for their preferences of conspecific versus heterospecific signals, however, we found that networks from allopatric populations were usually able to select against heterospecifics. We suggest that female preferences for aspects of conspecific male signals can result in a concomitant reduction in the likelihood that females will mate with heterospecifics. Consequently, even females in allopatry may discriminate against heterospecific mates depending on the nature of their preferences for conspecifics. Such a pattern could potentially explain cases where reproductive character displacement is expected, but not observed.

Social decision making involves the perception and processing of social stimuli, the subsequent evaluation of that information in the context of the individual's internal and external milieus to produce a decision, and then culminates in behavioural output informed by that decision. We examined brain networks in an anuran communication system that relies on acoustic signals to guide simple, stereotyped motor output. We used egr-1 mRNA expression to measure neural activation in male túngara frogs, Physalaemus pustulosus, following exposure to conspecific and heterospecific calls that evoke competitive or aggressive behaviour. We found that acoustically driven activation in auditory brainstem nuclei is transformed into activation related to sensory-motor interactions in the diencephalon, followed by motor-related activation in the telencephalon. Furthermore, under baseline conditions, brain nuclei typically have correlated egr-1 mRNA levels within brain divisions. Hearing conspecific advertisement calls increases correlations between anatomically distant brain divisions; no such effect was observed in response to calls that elicit aggressive behaviour. Neural correlates of social decision making thus take multiple forms: (i) a progressive shift from sensory to motor encoding from lower to higher stages of neural processing and (ii) the emergence of correlated activation patterns among sensory and motor regions in response to behaviourally relevant social cues.

Predators and parasites that eavesdrop on the mating signals of their prey often preferentially select individuals within a prey/host species that produce specific cues. Mechanisms driving such signal preferences are poorly understood. In the tungara frog Physalaemus pustulosus, conspecific females, frog-eating bats, and blood-sucking flies all prefer complex to simple mating calls. In this study we assess the natural signal variation in choruses in the wild and test two hypotheses for why eavesdroppers prefer complex calls: (1) prey quality: complex calls indicate better quality of prey/host, and (2) prey density: complex calls indicate higher prey/host density. Call complexity is not correlated with frog length, mass, or body condition, but it does signal higher abundance of prey/host. Thus, increased effectiveness of attack may have played a role favoring the preference for complex calls in eavesdropping heterospecifics.

One proposed mechanism of speciation is divergent sexual selection, whereby divergence in female preferences and male signals results in behavioural isolation. Despite the appeal of this hypothesis, evidence for it remains inconclusive. Here, we present several lines of evidence that sexual selection is driving behavioural isolation and speciation among populations of an Amazonian frog (Physalaemus petersi). First, sexual selection has promoted divergence in male mating calls and female preferences for calls between neighbouring populations, resulting in strong behavioural isolation. Second, phylogenetic analysis indicates that populations have become fixed for alternative call types several times throughout the species' range, and coalescent analysis rejects genetic drift as a cause for this pattern, suggesting that this divergence is due to selection. Finally, gene flow estimated with microsatellite loci is an average of 30 times lower between populations with different call types than between populations separated by a similar geographical distance with the same call type, demonstrating genetic divergence and incipient speciation. Taken together, these data provide strong evidence that sexual selection is driving behavioural isolation and speciation, supporting sexual selection as a cause for speciation in the wild.

We determined how social stimuli that vary in behavioral relevance differentially activate functional networks in the frog hypothalamus. As measured by egr-1 mRNA levels, activity in three hypothalamic nuclei varied with acoustic stimulus, and these responses were correlated with egr-1 responses in different auditory regions regardless of stimulus. The correlations among hypothalamic nuclei, however, varied as a function of the behavioral relevance of the stimuli. Thus relevant social cues shift the functional connectivity within the hypothalamus, consistent with principles that underlie the simultaneous processing of sensory information in cognitive tasks.

Female preferences for male mating signals are often evaluated on single parameters in isolation or small suites of characters. Most signals, however, are composites of many individual parameters. In this study we quantified multivariate traits in the advertisement call of the túngara frog, Physalaemus pustulosus. We represented the calls in multidimensional scaling space and chose nine test calls to represent the range of population variation. We then tested females for phonotactic preference between calls in each pair of the nine test calls. We used statistics developed for paired comparisons in such "round robin" competitions to evaluate the null hypothesis of equal attractiveness, and to examine the degree to which females responded to calls as being different from or similar to one another in attractiveness. We then examined the attractiveness of each test call relative to all other test calls as a function of their location in multivariate acoustic space (the acoustic landscape) to visualize sexual selection on calls. Finally, we used methods from cognitive psychology to illustrate the females' perception of call attractiveness in multivariate space, and compared this perceptual landscape to the acoustic landscape of quantitative call variation. We show that correlations between individual call characters are not strong and thus there are few biomechanical constraints on their independent evolution. Most call variables differed among males, and there was high repeatability of call characters within males. Females often discriminated between pairs of calls from the population, and there were significant differences among calls in their attractiveness. Female preferences for calls were not stabilizing. The region of the acoustic landscape that was most attractive to females included the mean call but was not centered around it. The females' perceptual or preference landscape did not correlate with the call's acoustic landscape, and female perception of calls decreased rather than enhanced call differences.

Females usually exhibit strong and unequivocal recognition of conspecific mating signals and reject those of other sympatric heterospecifics. However, most species are allopatric with one another, and the degree to which females recognize mating signals of allopatric species is more varied. Such mating signals are often rejected but are sometimes falsely recognized as conspecific. We studied the dynamics of mate recognition in female túngara frogs (Physalaemus pustulosus) in response to a series of calls that were intermediate between the conspecific and each of five allopatric-heterospecific calls: two that elicited recognition from females in previous studies and three that did not. This study shows that females perceive variation in allopatric mating signals in acontinuous manner with no evidence of perceptual category formation. The strength of recognition is predicted by how different the target stimulus is from the conspecific call within a series of calls. But the differences in recognition responses among call series are not predicted by the similarity of the call series to the conspecific call. The latter result suggests that the strength of recognition of allopatric signals might be influenced by processes of stimulus generalization and past evolutionary history.

Frogs are an ecologically diverse and phylogenetically ancient group of anuran amphibians that include important vertebrate cell and developmental model systems, notably the genus Xenopus. Here we report a high-quality reference genome sequence for the western clawed frog, Xenopus tropicalis, along with draft chromosome-scale sequences of three distantly related emerging model frog species, Eleutherodactylus coqui, Engystomops pustulosus, and Hymenochirus boettgeri. Frog chromosomes have remained remarkably stable since the Mesozoic Era, with limited Robertsonian (i.e., arm-preserving) translocations and end-to-end fusions found among the smaller chromosomes. Conservation of synteny includes conservation of centromere locations, marked by centromeric tandem repeats associated with Cenp-a binding surrounded by pericentromeric LINE/L1 elements. This work explores the structure of chromosomes across frogs, using a dense meiotic linkage map for X. tropicalis and chromatin conformation capture (Hi-C) data for all species. Abundant satellite repeats occupy the unusually long (~20 megabase) terminal regions of each chromosome that coincide with high rates of recombination. Both embryonic and differentiated cells show reproducible associations of centromeric chromatin and of telomeres, reflecting a Rabl-like configuration. Our comparative analyses reveal 13 conserved ancestral anuran chromosomes from which contemporary frog genomes were constructed.

Mate choice studies most often examine female preferences based on population responses, thus potentially overlooking individual differences in behavior. Moreover, such studies typically use invariant stimulus conditions to infer preferences. By using population responses and static stimulus presentations, it is difficult to thoroughly understand the complexity of the mate choice process, including variation present between individuals. Here, we investigated phonotactic mate choice behavior in female túngara frogs (Physalaemus pustulosus) in response to temporally dynamic presentations of male advertisement calls. We tested females on repeated trials to examine individual differences and found considerable variation in the extent to which females update their mate choice decisions. Females in our study were bimodally distributed and thus broadly classified as either committed or uncommitted to an initial mate approach. We compared body condition measures of females differing behaviorally and determined that females with larger residual body masses were more committed to initial mate choices than less massive individuals, despite the fact that all females were in reproductive condition and field collected in amplexus. Our results suggest that anuran phonotaxis, once considered to be a highly stereotyped behavior, is more complex and variable than previously thought. [ABSTRACT FROM PUBLISHER]

In most anurans, the production of advertisement calls is accompanied by the inflation of a vocal sac. Current functions of the vocal sac, however, are not fully understood, although several hypotheses have been proposed. One hypothesis suggests that the vocal sac decreases the intercall interval (i.e., increases call rate) by reinflating the lungs more rapidly than is possible with the buccal pump. We investigate this hypothesis by analyzing audio and video recordings of calling túngara frogs. We compare the first two call bouts emitted by an originally uninflated male. The first call bout requires lung inflation via buccal pumping, but in the second, the male is already inflated because of capture of air and reinflation of the lungs by the vocal sac. Lung inflation to typical field levels requires 26–51 buccal pumps, which takes at least 4.4 s. This estimate is more than 2.5 times the typical intercall interval with lung reinflation via a vocal sac (ca. 1.7 s). Evidence from phonotaxis tests demonstrates that these differences in intercall intervals are salient to females and that female Physalaemus pustulosus prefer the shorter intercall interval/higher call rate. Acoustic analyses demonstrate that the first call of bout 1, which requires buccal pumping, is usually shorter, of lower amplitude, and spans a smaller frequency range than the first call of bout 2, which does not require buccal pumping. Because females prefer longer, more intense calls, these results suggest that the vocal sac not only increases call rate but also allows males to produce more calls of increased attractiveness to females. [ABSTRACT FROM AUTHOR]

In most sexually reproducing animals, the behavior of one or both sexes during courtship critically influences the success at mating of the opposite sex. This behavior is often interpreted as “mate choice,” and there is great interest in why such choices are exercised. The explanation for the evolution of mate choice that has received the most attention and generated the most controversy is based on assumed genetic effects. In this study, we investigated whether female túngara frogs, which choose mates based on acoustic cues, have a preference for genetically less related males. Specifically, we determine if there is disassortive mating based on microsatellite markers, if there is information in the advertisement call that could be used to assess genetic similarity, and if females exhibit acoustic-based mating preferences that would promote choice for genetic diversity. Using seven microsatellite markers, we found no correlation of male call similarity and male genetic relatedness. Female choice experiments showed no female preference for calls of less related males, and there was no evidence for inbreeding avoidance in the field. Our results do not support the hypothesis of mate choice based on information about genetic relatedness conveyed by acoustic signals in túngara frogs. [ABSTRACT FROM AUTHOR]

The human music faculty might have evolved from rudimentary components that occur in non-human animals. The evolutionary history of these rudimentary perceptual features is not well understood and rarely extends beyond a consideration of vertebrates that possess a cochlea. One such antecedent is a preferential response to what humans perceive as consonant harmonic sounds, which are common in many animal vocal repertoires. We tested the phonotactic response of female túngara frogs (Physalaemus pustulosus) to variations in the frequency ratios of their harmonically structured mating call to determine whether frequency ratio influences attraction to acoustic stimuli in this vertebrate that lacks a cochlea. We found that the ratio of frequencies present in acoustic stimuli did not influence female response. Instead, the amount of inner ear stimulation predicted female preference behaviour. We conclude that the harmonic relationships that characterize the vocalizations of these frogs did not evolve in response to a preference for frequency intervals with low-integer ratios. Instead, the presence of harmonics in their mating call, and perhaps in the vocalizations of many other animals, is more likely due to the biomechanics of sound production rather than any preference for 'more musical' sounds. [ABSTRACT FROM AUTHOR]