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Abstract Species worldwide are disappearing in the most devastating mass extinction in human history and one of the six most profound extinctions in the history of life. Amphibians are greatly affected, approximately one third of living species are threatened, and many others are extinct. One of the main causes of amphibian species extinctions and population declines is the emerging infectious disease chytridiomycosis, caused by the fungusBatrachochytrium dendrobatidis(Bd). Although some species are somewhat tolerant of the disease, the non-lethal effects of the infection with Bd and their short or long term consequences are poorly understood. In these species there is the potential for behavioral responses to mitigate the spread of the fungus. Here we show that in túngara frogs, infection status influences the males’ mating calls. These infection-induced changes in the quality of males’ mating calls ultimately reduce the calls’ attractiveness to females making females less likely to respond to and thus mate with infected males. More broadly, our results imply that females might avoid mating with disease-infected males by assessing the acoustic signal only, and that such recruitment of behavioral responses might potentially ameliorate some of the effects of this sixth mass extinction. Lay summaryChytridiomycosis is an amphibian disease well known for its lethal effects. Túngara frogs are infected in nature, but seem to be resistant to the disease. Here we show that chytridiomycosis has non-lethal behavioral effects on túngara frogs. Females discriminate against infected males by assessing only their acoustic signal. The mating call of a male that is not infected with the disease is more attractive to females than the call of that same male when he is infected. 

Abstract Acoustic communication signals are important for species recognition and mate attraction across numerous taxa. For instance, most of the thousands of species of frogs have a species-specific advertisement call that females use to localize and discriminate among potential mates. Thus, the acoustic structure of the advertisement call is critical for reproductive success. The acoustic structure of calls will generally diverge over evolutionary time and can be influenced by the calls of sympatric species. While many studies have shown the influence of geography on contemporary call variation in populations of frogs, no study has compared the acoustic structure of frog calls across many species to ask whether we can detect an influence of divergence time and overall geographic overlap on the differences in acoustic structure of species-typical calls that we observe now. To this end, we compared acoustic features of the calls of 225 species of frogs within 4 families. Furthermore, we used a behavioral assay from 1 species of frog to determine which acoustic features to prioritize in our large-scale analyses. We found evidence that both phylogeny (time) and geography (place) relate to advertisement call acoustics albeit with large variation in these relationships across the 4 families in the analysis. Overall, these results suggest that, despite the many ecological and evolutionary forces that influence call structure, the broad forces of time and place can shape aspects of advertisement call acoustics. 

Abstract Sexual selection can result in the evolution of extreme armaments and ornaments, and the development and maintenance of these traits can come at a considerable cost. These costs have been implicated in enforcing an upper limit on trait divergence and promoting condition-dependent traits, such that only individuals in sufficiently high condition can effectively wield these armaments and advertise these ornaments. Numerous studies demonstrate the condition-dependence of sexually selected traits, especially those used by males to advertise to females. In this study, we investigated condition-dependent mating calls in the túngara frogPhysalaemus(= Engystomops)pustulosus. We manipulated male condition in the laboratory over a nine-day period by restricting food availability. We then documented: the relationship between male condition (the relative change in body mass from night 1 to night 9) and acoustic parameters of his mating call; how male condition influenced the male’s responses to call playbacks; and finally, how male condition influenced the attractiveness of the male’s calls to females. Males who were not fed during this period showed significant changes in call frequency, duration, and amplitude. In response to playbacks, unfed males called less, and made fewer complex calls. Finally, in phonotaxis experiments, females were more attracted to the calls of unfed males on night 1 to the calls of the same males on night 9. Fed males, on the other hand, showed no significant differences between nights 1 and 9 in call parameters, calling effort, and call attractiveness. This study shows the pervasive effects of condition on three aspects of sexual communication: signal parameters, behavioral response to vocal competition, and mating call attractiveness. 

Abstract For chorusing males, optimally timing their calls relative to nearby rivals’ calls and fluctuations in background chorus noise is crucial for reproductive success. A caller’s acoustic environment will vary by chorus density and the properties of his chorus-mates’ calls and will fluctuate unpredictably due to chorusing dynamics emerging among his chorus-mates. Thus, callers must continuously monitor moment-to-moment fluctuations in the acoustic scene they perceive at the chorus for advantageous times to call. In live experimental choruses, we investigated the factors influencing túngara frog call-timing responses to chorus-mates’ calls on an interaction-by-interaction basis, revealing that intrinsic and extrinsic factors influenced call-timing decisions. Callers were more likely to overlap calls from smaller chorus-mates and chorus-mates at intermediate distances, as well as calls containing lower frequencies and exhibiting lower final amplitude minima. Consequently, variation among males in call properties led to variation in levels of call-interference received when calling in the same social environment. Additionally, callers were more likely to overlap chorus-mates’ calls after experiencing extended periods of inhibition and were less likely to overlap synchronized chorus-mates’ calls relative to single calls. In chorusing species, female choice is influenced by inter-caller dynamics, selecting for male call-timing strategies which, in turn, constitute the selective environment further refining these same strategies. Thus, understanding the specific factors driving call-timing decisions is essential for understanding how sexual selection operates in chorusing taxa. 

Male frogs court females from within crowded choruses, selecting for mechanisms allowing them to call at favourable times relative to the calls of rivals and background chorus noise. To accomplish this, males must continuously evaluate the fluctuating acoustic scene generated by their competitors for opportune times to call. Túngara frogs produce highly frequency- and amplitude-modulated calls from within dense choruses. We used similarly frequency- and amplitude-modulated playback tones to investigate the sensory basis of their call-timing decisions. Results revealed that different frequencies present throughout this species’ call differed in their degree of call inhibition, and that lower-amplitude tones were less inhibitory. Call-timing decisions were then driven by fluctuations in inhibition arising from underlying frequency- and amplitude-modulation patterns, with tone transitions that produced steeper decreases in inhibition having higher probabilities of triggering calls. Interactions between the varied behavioural sensitivities to different conspecific call frequencies revealed here, and the stereotyped amplitude- and frequency-modulation patterns present in this species’ calls, can explain previously surprising patterns observed in túngara frog choruses. This highlights the importance of understanding the specific sensory drivers underpinning conspecific signalling interactions, and reveals how sensory systems can mediate the interplay between signal perception and production to facilitate adaptive communication strategies. 

Abstract Communication signals by both human and non-human animals are often interrupted in nature. One advantage of multimodal cues is to maintain the salience of interrupted signals. We studied a frog that naturally can have silent gaps within its call. Using video/audio-playbacks, we presented females with interrupted mating calls with or without a simultaneous dynamic (i.e., inflating and deflating) vocal sac and tested whether multisensory cues (noise and/or dynamic vocal sac) inserted into the gap can compensate an interrupted call. We found that neither inserting white noise into the silent gap of an interrupted call nor displaying the dynamic vocal sac in that same gap restored the attraction of the call equivalent to that of a complete call. Simultaneously presenting a dynamic vocal sac along with noise in the gap, however, compensated the interrupted call, making it as attractive as a complete call. Our results demonstrate that the dynamic visual sac compensates for noise interference. Such novel multisensory integration suggests that multimodal cues can provide insurance against imperfect sender coding in a noisy environment, and the communication benefits to the receiver from multisensory integration may be an important selective force favoring multimodal signal evolution. 

For complex communication signals, it is often difficult to identify the information-bearing elements and their parameters necessary to elicit functional behavior. Consequently, it may be difficult to design stimuli that test how neurons contribute to communicative processing. For tu´ngara frogs (Physalaemus pustulosus), however, previous behavioral testing with numerous stimuli showed that a particular frequency modulated (FM) transition in the male call is required to elicit phonotaxis and vocal responses. Modeled on such behavioral experiments, we used awake in vivo recordings of single units in the midbrain to determine if their excitation was biased to behaviorally important FM parameters. Comparisons of stimulus driven action potentials revealed greatest excitation to the behaviorally important FM transition: a downward FM sweep or step that crosses ~600 Hz. Previous studies using long-duration acoustic exposure found immediate early gene expression in many midbrain neurons to be most sensitive to similar FM. However, those data could not determine if FM coding was accomplished by the population and/or individual neurons. Our data suggest both coding schemes could operate, as 1) individual neurons are more sensitive to the behaviorally significant FM transition and 2) when single unit recordings are analytically combined across cells, the combined code can produce high stimulus discrimination (FM vs. noise driven excitation), approaching that found in behavioral discrimination of call vs. noise.