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As species change through evolutionary time, the neurological and morphological structures that underlie behavioral systems typically remain coordinated. This is especially important for communication systems, in which these structures must remain coordinated both within and between senders and receivers for successful information transfer. The acoustic communication of anurans ("frogs") offers an excellent system to ask when and how such coordination is maintained, and to allow researchers to dissociate allometric effects from independent correlated evolution. Anurans constitute one of the most speciose groups of vocalizing vertebrates, and females typically rely on vocalizations to localize males for reproduction. Here, we compile and compare data on various aspects of auditory morphology, hearing sensitivity, and call-dominant frequency across 81 species of anurans. We find robust, phylogenetically independent scaling effects of body size for all features measured. Furthermore, after accounting for body size, we find preliminary evidence that morphological evolution beyond allometry can correlate with hearing sensitivity and dominant frequency. These data provide foundational results regarding constraints imposed by body size on communication systems and motivate further data collection and analysis using comparative approaches across the numerous anuran species., (© 2021 S. Karger AG, Basel.)

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.)

In animal communication, receivers benefit from signals providing reliable information on signalers' traits of interest. Individuals involved in conflicts, such as competition between rivals, should pay particular attention to cues that are "unfakeable" by the senders due to the intrinsic properties of the production process. In bioacoustics, the best-known example of such "index signals" is the relationship between a sender's body size and the dominant frequency of their vocalizations. Dominant frequency may, however, not only depend on an animal's morphology but also on the interaction between the sound production system and its immediate environment. Here, we experimentally altered the environment surrounding calling frogs and assessed its impact on the signal produced. Our results show that frogs that are floating are able to inflate their vocal sacs fully and that this change in inflation level is correlated with a decrease of call dominant frequency.

Unlike in terrestrial animals, the boundary between internal (e.g., hormones) and external (e.g., social) stimulation can be blurred for aquatic and amphibious species. When chemicals such as hormones and glandular secretions leach into the water, they can further interact with other signaling systems, creating multimodal stimuli. It is unclear, however, whether water-borne chemical secretions from courting male frogs affect the physiology and behavior of their rivals. In order to address this question we first established non-invasive, continuous sampling methods for simultaneously measuring both hormones and behavior in amphibious species. Then, we examined whether interactions between water-borne chemical secretions and conspecific calls affect reproductive behavior and physiology (testosterone and corticosterone) of courting male túngara frogs. Our results demonstrate that conspecific acoustic stimulation alone increases locomotor activity, decreases latency to call, and increases calling behavior but does not alter the amount of hormones excreted. In response to water containing chemical secretions from rivals, but in the absence of calls from other males, males excrete more testosterone. Interestingly, the combined acoustic and chemical stimulus causes a multiplicative increase in both calling behavior and hormonal excretion. Taken together, our results suggest that a multimodal chemical-acoustic stimulus physiologically primes males for aggressive behavior., (Published by Elsevier Inc.)

Sexual selection driven by mate choice has generated some of the most astounding diversity in nature, suggesting that population-level preferences should be strong and consistent over many generations. On the other hand, mating preferences are among the least repeatable components of an individual animal's phenotype, suggesting that consistency should be low across an animal's lifetime. Despite decades of intensive study of sexual selection, there is almost no information about the strength and consistency of preferences across many years. In this study, we present the results of more than 5,000 mate choice tests with a species of wild frog conducted over 19 consecutive years. Results show that preferences are positive and strong and vary little across years. This consistency occurs despite the fact that there are substantial differences among females in their strength of preference. We also suggest that mate preferences in populations that are primarily the result of sensory exploitation might be more stable over time than preferences that are primarily involved in assessing male quality.

Urbanization can cause species to adjust their sexual displays, because the effectiveness of mating signals is influenced by environmental conditions. Despite many examples that show that mating signals in urban conditions differ from those in rural conditions, we do not know whether these differences provide a combined reproductive and survival benefit to the urban phenotype. Here we show that male túngara frogs have increased the conspicuousness of their calls, which is under strong sexual and natural selection by signal receivers, as an adaptive response to city life. The urban phenotype consequently attracts more females than the forest phenotype, while avoiding the costs that are imposed by eavesdropping bats and midges, which we show are rare in urban areas. Finally, we show in a translocation experiment that urban frogs can reduce risk of predation and parasitism when moved to the forest, but that forest frogs do not increase their sexual attractiveness when moved to the city. Our findings thus reveal that urbanization can rapidly drive adaptive signal change via changes in both natural and sexual selection pressures.

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.)

The neuropeptide arginine vasotocin (AVT) promotes sexual advertisement and influences vocalization structure in male anuran amphibians. In the present study, we used wild túngara frogs (Physalaemus pustulosus) to investigate the effects of AVT on phonotaxis in males and females-thereby controlling for potential task differences between the sexes. Using a combined within- and between-subjects design, we showed that acoustic choice behavior in female frogs is not influenced by injection per se (vehicle) or by AVT. Latency to choice in females, however, tends to decrease after AVT injection, supporting the hypothesis that AVT promotes female sexual arousal. In contrast, male choice behavior and latencies are negatively impacted by injection (vehicle) but rescued to pre-injection levels if administered with AVT. The sexes differed in area restricted searching (ARS) following choice-a measure of locomotor perseverance-with females but not males exhibiting ARS. AVT did not influence ARS behavior but ARS frequency was positively associated with the attractiveness of the acoustic stimulus. Finally, we showed that a female's latency behavior is correlated with her partner's behavior. Collectively we show that AVT promotes phonotaxis in both sexes in a dimorphic manner-a result that is consistent with sex differences in the neural vasotocin system.

Perceptually, grouping sounds based on their sources is critical for communication. This is especially true in túngara frog breeding aggregations, where multiple males produce overlapping calls that consist of an FM 'whine' followed by harmonic bursts called 'chucks'. Phonotactic females use at least two cues to group whines and chucks: whine-chuck spatial separation and sequence. Spatial separation is a primitive cue, whereas sequence is schema-based, as chuck production is morphologically constrained to follow whines, meaning that males cannot produce the components simultaneously. When one cue is available, females perceptually group whines and chucks using relative comparisons: components with the smallest spatial separation or those closest to the natural sequence are more likely grouped. By simultaneously varying the temporal sequence and spatial separation of a single whine and two chucks, this study measured between-cue perceptual weighting during a specific grouping task. Results show that whine-chuck spatial separation is a stronger grouping cue than temporal sequence, as grouping is more likely for stimuli with smaller spatial separation and non-natural sequence than those with larger spatial separation and natural sequence. Compared to the schema-based whine-chuck sequence, we propose that spatial cues have less variance, potentially explaining their preferred use when grouping during directional behavioral responses.

The world is a noisy place, and animals have evolved a myriad of strategies to communicate in it. Animal communication signals are, however, often multimodal; their components can be processed by multiple sensory systems, and noise can thus affect signal components across different modalities. We studied the effect of environmental noise on multimodal communication in the túngara frog (Physalaemus pustulosus). Males communicate with rivals using airborne sounds combined with call-induced water ripples. We tested males under control as well as noisy conditions in which we mimicked rain- and wind-induced vibrations on the water surface. Males responded more strongly to a multimodal playback in which sound and ripples were combined, compared to a unimodal sound-only playback, but only in the absence of rain and wind. Under windy conditions, males decreased their response to the multimodal playback, suggesting that wind noise interferes with the detection of rival ripples. Under rainy conditions, males increased their response, irrespective of signal playback, suggesting that different noise sources can have different impacts on communication. Our findings show that noise in an additional sensory channel can affect multimodal signal perception and thereby drive signal evolution, but not always in the expected direction.

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.

In humans and some nonhuman vertebrates, a sound containing brief silent gaps can be rendered perceptually continuous by inserting noise into the gaps. This so-called "continuity illusion" arises from a phenomenon known as "auditory induction" and results in the perception of complete auditory objects despite fragmentary or incomplete acoustic information. Previous studies of auditory induction in gray treefrogs (Hyla versicolor and H. chrysoscelis) have demonstrated an absence of this phenomenon. These treefrog species produce pulsatile (noncontinuous) vocalizations, whereas studies of auditory induction in other taxa, including humans, often present continuous sounds (e.g., frequency-modulated sweeps). This study investigated the continuity illusion in a frog (Physalaemus pustulosus) with an advertisement vocalization that is naturally continuous and thus similar to the tonal sweeps used in human psychophysical studies of auditory induction. In a series of playback experiments, female subjects were presented with sets of stimuli that included complete calls, calls with silent gaps, and calls with silent gaps filled with noise. The results failed to provide evidence of auditory induction. Current evidence, therefore, suggests that mammals and birds experience auditory induction, but frogs may not. This emerging pattern of taxonomic differences is considered in light of potential methodological, neurophysiological, and functional explanations., ((c) 2016 APA, all rights reserved).)

Mate choice models derive from traditional microeconomic decision theory and assume that individuals maximize their Darwinian fitness by making economically rational decisions. Rational choices exhibit regularity, whereby the relative strength of preferences between options remains stable when additional options are presented. We tested female frogs with three simulated males who differed in relative call attractiveness and call rate. In binary choice tests, females' preferences favored stimulus caller B over caller A; however, with the addition of an inferior "decoy" C, females reversed their preferences and chose A over B. These results show that the relative valuation of mates is not independent of inferior alternatives in the choice set and therefore cannot be explained with the rational choice models currently used in sexual selection theory., (Copyright © 2015, American Association for the Advancement of Science.)

Sexual communication can evolve in response to sexual selection, and it can also cause behavioral reproductive isolation between populations and thus drive speciation. Anurans are an excellent system to investigate these links between behavior and evolution because we have detailed knowledge of how neural mechanisms generate behavioral preferences for calls and how these preferences then generate selection on call variation. But we know far less about the physical mechanisms of call production, especially how different laryngeal morphologies generate call variation. Here we review studies of a group of species that differ in the presence of a secondary call component that evolved under sexual selection. We discuss how the larynx produces this call component, and how laryngeal morphology generates sexual selection and can contribute to speciation., (Copyright © 2014. Published by Elsevier Ltd.)

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.)

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.

Animal choruses, such as those found in insects and frogs, are often intermittent. Thus, females sampling males in the chorus might have to remember the location of the potential mates' calls during periods of silence. Although a number of studies have shown that frogs use and prefer multimodal mating signals, usually acoustic plus visual, it is not clear why they do so. Here we tested the hypothesis that preference for multimodal signals over unimodal signals might be due to multimodal signals instantiating longer memories than unimodal signals, particularly during the inter‐chorus intervals.We tested this hypothesis in serrate‐legged small treefrogs Kurixalus odontotarsus whose males produce advertisement calls accompanied by conspicuous vocal sac inflation. Females were tested with acoustic and acoustic + visual (video of inflating‐deflating vocal sac) mating calls.We found that females prefer multimodal calls over unimodal, audio‐only calls. Furthermore, multimodal calls are still preferred after a silent period of up to 30 s, a time that spans the average silent period of the chorus. This was not true of unimodal calls.Our results demonstrate that a multimodal signal can engage longer working memory than a unimodal signal, and thus female memory might favour the evolution of multimodal signals in males through sexual selection. Selection might also favour female preference for multimodal signals if longer memory facilitates mate searching and assessment. Our study does not allow us to elucidate the sequence of evolution of this trait and preference. [ABSTRACT FROM AUTHOR]