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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 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 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. 

Taking an evolutionary approach to the question of beauty, we discuss the expression and perception of sexual beauty across the animal kingdom. Animals experience beauty in their brains, and animal brains are tuned to features of the environment most relevant to their survival. Over evolutionary time, sexually reproducing animals have exploited that tuning to maximize their attractiveness to the opposite sex, often leading to extreme courtship traits and behaviors. These are the traits of sexual beauty. Combining modern principles of neuroscience and neuroaesthetics with established principles of evolutionary biology, we aim to understand the biological basis and evolution of beauty in all animals, including ourselves. 

Abstract To forage efficiently, animals should selectively attend to and remember the cues of food that best predict future meals. One hypothesis is that animals with different foraging strategies should vary in their reliance on spatial versus feature cues. Specifically, animals that store food in dispersed caches or that feed on spatially stable food, such as fruits or flowers, should be relatively biased towards learning a meal’s location, whereas predators that hunt mobile prey should instead be relatively biased towards learning feature cues such as odor or sound. Several authors have predicted that nectar-feeding and fruit-feeding bats would rely relatively more on spatial cues, whereas closely related predatory bats would rely more on feature cues, yet no experiment has compared these two foraging strategies under the same conditions. To test this hypothesis, we compared learning in the frugivorous bat, Artibeus jamaicensis, and the predatory bat, Lophostoma silvicolum, which hunts katydids using acoustic cues. We trained bats to find food paired with a unique and novel odor, sound, and location. To assess which cues each bat had learned, we then dissociated these cues to create conflicting information. Rather than finding that the frugivore and predator clearly differ in their relative reliance on spatial versus feature cues, we found that both species used spatial cues over sounds or odors in subsequent foraging decisions. We interpret these results alongside past findings on how foraging animals use spatial cues versus feature cues, and explore why spatial cues may be fundamentally more rich, salient, or memorable. 

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. 

BACKGROUND Charles Darwin’s  Descent of Man, and Selection in Relation to Sex  tackled the two main controversies arising from the Origin of Species:  the evolution of humans from animal ancestors and the evolution of sexual ornaments. Most of the book focuses on the latter, Darwin’s theory of sexual selection. Research since supports his conjecture that songs, perfumes, and intricate dances evolve because they help secure mating partners. Evidence is overwhelming for a primary role of both male and female mate choice in sexual selection—not only through premating courtship but also through intimate interactions during and long after mating. But what makes one prospective mate more enticing than another? Darwin, shaped by misogyny and sexual prudery, invoked a “taste for the beautiful” without speculating on the origin of the “taste.” How to explain when the “final marriage ceremony” is between two rams? What of oral sex in bats, cloacal rubbing in bonobos, or the sexual spectrum in humans, all observable in Darwin’s time? By explaining desire through the lens of those male traits that caught his eyes and those of his gender and culture, Darwin elided these data in his theory of sexual evolution. Work since Darwin has focused on how traits and preferences coevolve. Preferences can evolve even if attractive signals only predict offspring attractiveness, but most attention has gone to the intuitive but tenuous premise that mating with gorgeous partners yields vigorous offspring. By focusing on those aspects of mating preferences that coevolve with male traits, many of Darwin’s influential followers have followed the same narrow path. The sexual selection debate in the 1980s was framed as “good genes versus runaway”: Do preferences coevolve with traits because traits predict genetic benefits, or simply because they are beautiful? To the broader world this is still the conversation. ADVANCES Even as they evolve toward ever-more-beautiful signals and healthier offspring, mate-choice mechanisms and courter traits are locked in an arms race of coercion and resistance, persuasion and skepticism. Traits favored by sexual selection often do so at the expense of chooser fitness, creating sexual conflict. Choosers then evolve preferences in response to the costs imposed by courters. Often, though, the current traits of courters tell us little about how preferences arise. Sensory systems are often tuned to nonsexual cues like food, favoring mating signals resembling those cues. And preferences can emerge simply from selection on choosing conspecifics. Sexual selection can therefore arise from chooser biases that have nothing to do with ornaments. Choice may occur before mating, as Darwin emphasized, but individuals mate multiple times and bias fertilization and offspring care toward favored partners. Mate choice can thus occur in myriad ways after mating, through behavioral, morphological, and physiological mechanisms. Like other biological traits, mating preferences vary among individuals and species along multiple dimensions. Some of this is likely adaptive, as different individuals will have different optimal mates. Indeed, mate choice may be more about choosing compatible partners than picking the “best” mate in the absolute sense. Compatibility-based choice can drive or reinforce genetic divergence and lead to speciation. The mechanisms underlying the “taste for the beautiful” determine whether mate choice accelerates or inhibits reproductive isolation. If preferences are learned from parents, or covary with ecological differences like the sensory environment, then choice can promote genetic divergence. If everyone shares preferences for attractive ornaments, then choice promotes gene flow between lineages. OUTLOOK Two major trends continue to shift the emphasis away from male “beauty” and toward how and why individuals make sexual choices. The first integrates neuroscience, genomics, and physiology. We need not limit ourselves to the feathers and dances that dazzled Darwin, which gives us a vastly richer picture of mate choice. The second is that despite persistent structural inequities in academia, a broader range of people study a broader range of questions. This new focus confirms Darwin’s insight that mate choice makes a primary contribution to sexual selection, but suggests that sexual selection is often tangential to mate choice. This conclusion challenges a persistent belief with sinister roots, whereby mate choice is all about male ornaments. Under this view, females evolve to prefer handsome males who provide healthy offspring, or alternatively, to express flighty whims for arbitrary traits. But mate-choice mechanisms also evolve for a host of other reasons Understanding mate choice mechanisms is key to understanding how sexual decisions underlie speciation and adaptation to environmental change. New theory and technology allow us to explicitly connect decision-making mechanisms with their evolutionary consequences. A century and a half after Darwin, we can shift our focus to females and males as choosers, rather than the gaudy by-products of mate choice. Mate choice mechanisms across domains of life. Sensory periphery for stimulus detection (yellow), brain for perceptual integration and evaluation (orange), and reproductive structures for postmating choice among pollen or sperm (teal). ILLUSTRATION: KELLIE HOLOSKI/ SCIENCE