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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.

 

Frogs are an ecologically diverse and phylogenetically ancient group of anuran amphibians that include important vertebrate cell and developmental model systems, notably the genusXenopus. 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, andHymenochirus 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 forX. tropicalisand 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.

 

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. 

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 Females of many species choose mates using multiple sensory modalities. Multimodal noise may arise, however, in dense aggregations of animals communicating via multiple sensory modalities. Some evidence suggests multimodal signals may not always improve receiver decision-making performance. When sensory systems process input from multimodal signal sources, multimodal noise may arise and potentially complicate decision-making due to the demands on cognitive integration tasks. We tested female túngara frog, Physalaemus (=Engystomops) pustulosus, responses to male mating signals in noise from multiple sensory modalities (acoustic and visual). Noise treatments were partitioned into three categories: acoustic, visual, and multimodal. We used natural calls from conspecifics and heterospecifics for acoustic noise. Robotic frogs were employed as either visual signal components (synchronous vocal sac inflation with call) or visual noise (asynchronous vocal sac inflation with call). Females expressed a preference for the typically more attractive call in the presence of unimodal noise. However, during multimodal signal and noise treatments (robofrogs employed with background noise), females failed to express a preference for the typically attractive call in the presence of conspecific chorus noise. We found that social context and temporal synchrony of multimodal signaling components are important for multimodal communication. Our results demonstrate that multimodal signals have the potential to increase the complexity of the sensory scene and reduce the efficacy of female decision making. 

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 

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. 

One hundred fifty years ago Darwin published The Descent of Man, and Selection in Relation to Sex , in which he presented his theory of sexual selection with its emphasis on sexual beauty. However, it was not until 50 y ago that there was a renewed interest in Darwin’s theory in general, and specifically the potency of mate choice. Darwin suggested that in many cases female preferences for elaborately ornamented males derived from a female’s taste for the beautiful, the notion that females were attracted to sexual beauty for its own sake. Initially, female mate choice attracted the interest of behavioral ecologists focusing on the fitness advantages accrued through mate choice. Subsequent studies focused on sensory ecology and signal design, often showing how sensory end organs influenced the types of traits females found attractive. Eventually, investigations of neural circuits, neurogenetics, and neurochemistry uncovered a more complete scaffolding underlying sexual attraction. More recently, research inspired by human studies in psychophysics, behavioral economics, and neuroaesthetics have provided some notion of its higher-order mechanisms. In this paper, I review progress in our understanding of Darwin’s conjecture of “a taste for the beautiful” by considering research from these diverse fields that have conspired to provide unparalleled insight into the chooser’s mate choices.