Title: Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice
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. more »« less
Communication systems often include a variety of components,
including those that span modalities, which may facilitate detection
and decision-making. For example, female tungara frogs and fringe-lipped
bats generally rely on acoustic mating signals to find male
tungara frogs in a mating or foraging context, respectively. However,
two additional cues (vocal sac inflation and water ripples) can
enhance detection and choice behavior. To date, we do not know
the natural variation and covariation of these three components. To
address this, we made detailed recordings of calling males, including
call amplitude, vocal sac volume and water ripple height, in 54 frogs
(2430 calls). We found that all three measures correlated, with the
strongest association between the vocal sac volume and call
amplitude. We also found that multimodal models predicted the
mass of calling males better than unimodal models. These results
demonstrate how multimodal components of a communication system
relate to each other and provide an important foundation for future
studies on how receivers integrate and compare complex displays.
Taylor, Ryan C.; Wilhite, Kyle O.; Ludovici, Rosalind J.; Mitchell, Kelsey M.; Halfwerk, Wouter; Page, Rachel A.; Ryan, Michael J.; Hunter, Kimberly L.(
, Journal of Experimental Biology)
Noise is a common problem in animal communication. We know little, however, about how animals communicate in noise using multimodal signals. Multimodal signals are hypothesized to be favoured by evolution because they increase the efficacy of detection/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.
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.
Leary, Christopher J; Crocker-Buta, Sarah; Holloway, Ashli; Kennedy, Joseph G(
, Integrative and Comparative Biology)
Synopsis Adrenal glucocorticoids (GCs) are increasingly recognized as important modulators of male courtship signals, suggesting that circulating levels of these steroids can play a central role in sexual selection. However, few studies have examined whether GC-mediated effects on male sexual signals actually impact mate choice by females. Here, we examine how corticosterone (CORT)-mediated changes in the vocalizations of male green treefrogs, Dryophytes cinereus, influence attractiveness to females. In this species, agonistic acoustic signaling between rival males competing for mates increases circulating CORT levels in contest losers. Acute elevations in CORT, in turn, decrease the duration of male advertisement calls and increase the latency between successive calls, resulting in a net reduction in vocal effort (the amount of signaling per unit time) that occurs independently of changes in circulating androgens. Based on known preferences for acoustic features in D. cinereus, and other anuran species, the direction of CORT-mediated effects on temporal call characteristics is expected to compromise attractiveness to females, but whether they are of sufficient magnitude to impact female mate choice decisions is unclear. To examine whether CORT-mediated effects on male advertisement calls reduce attractiveness to females, we broadcast vocalizations in dual speaker playback experiments approximating the mean and 1 SD above and below the mean call duration and vocal effort values (the two primary vocal features impacted by elevated CORT) of males with low and high CORT levels. Results revealed strong preferences by females for the calls characteristic of males with low CORT in tests using the approximate mean and 1 SD above the mean call duration and vocal effort values, but females did not show a preference for calls of males with low CORT in trials using call values approximating 1 SD below the mean. Overall, females preferred males with signal traits predictive of low CORT, however this effect was nonlinear with attenuated preferences when signal alternatives differed only marginally indicating a possible thresholding effect. Specifically, females appeared to discriminate between males with low versus high CORT based primarily on differences in call rates associated with CORT-mediated changes in call duration and vocal effort. Our results highlight that changes in circulating CORT during male–male vocal interactions can decrease attractiveness to females, suggesting that circulating levels of CORT can play a critical role in both intra- and intersexual selection.
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
Coss, Derek A, Ryan, Michael J, Page, Rachel A, Hunter, Kimberly L, and Taylor, Ryan C. Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice. Retrieved from https://par.nsf.gov/biblio/10350468. Behavioral Ecology . Web. doi:10.1093/beheco/arac061.
Coss, Derek A, Ryan, Michael J, Page, Rachel A, Hunter, Kimberly L, & Taylor, Ryan C. Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice. Behavioral Ecology, (). Retrieved from https://par.nsf.gov/biblio/10350468. https://doi.org/10.1093/beheco/arac061
Coss, Derek A, Ryan, Michael J, Page, Rachel A, Hunter, Kimberly L, and Taylor, Ryan C.
"Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice". Behavioral Ecology (). Country unknown/Code not available. https://doi.org/10.1093/beheco/arac061.https://par.nsf.gov/biblio/10350468.
@article{osti_10350468,
place = {Country unknown/Code not available},
title = {Can you hear/see me? Multisensory integration of signals does not always facilitate mate choice},
url = {https://par.nsf.gov/biblio/10350468},
DOI = {10.1093/beheco/arac061},
abstractNote = {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.},
journal = {Behavioral Ecology},
author = {Coss, Derek A and Ryan, Michael J and Page, Rachel A and Hunter, Kimberly L and Taylor, Ryan C},
editor = {Candolin, Ulrika}
}
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