skip to main content

Title: Glucocorticoid-Mediated Changes in Male Green Treefrog Vocalizations Alter Attractiveness to Females
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 more » 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. « less
; ; ;
Award ID(s):
Publication Date:
Journal Name:
Integrative and Comparative Biology
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Researchers have long examined the structure of animal advertisement signals, but comparatively little is known about how often these signals are repeated and what factors predict variation in signaling rate across species. Here, we focus on acoustic advertisement signals to test the hypothesis that calling males experience a tradeoff between investment in the duration or complexity of individual calls and investment in signaling over long time periods. This hypothesis predicts that the number of signals that a male produces per 24 h will negatively correlate with (1) the duration of sound that is produced in each call (the sum of all pulses) and (2) the number of sound pulses per call. To test this hypothesis, we measured call parameters and the number of calls produced per 24 h in 16 species of sympatric phaneropterine katydids from the Panamanian rainforest. This assemblage also provided us with the opportunity to test a second taxonomically specific hypothesis about signaling rates in taxa such as phaneropterine katydids that transition from advertisement calls to mating duets to facilitate mate localization. To establish duets, male phaneropterine katydids call and females produce a short acoustic reply. These duets facilitate searching by males, females, or both sexes,more »depending on the species. We test the hypothesis that males invest either in calling or in searching for females. This hypothesis predicts a negative relationship between how often males signal over 24 h and how much males move across the landscape relative to females. For the first hypothesis, there was a strong negative relationship between the number of signals and the duration of sound that is produced in each signal, but we find no relationship between the number of signals produced per 24 h and the number of pulses per signal. This result suggests the presence of cross-taxa tradeoffs that limit signal production and duration, but not the structure of individual signals. These tradeoffs could be driven by energetic limitations, predation pressure, signal efficacy, or other signaling costs. For the second hypothesis, we find a negative relationship between the number of signals produced per day and proportion of the light trap catch that is male, likely reflecting males investing either in calling or in searching. These cross-taxa relationships point to the presence of pervasive trade-offs that fundamentally shape the spatial and temporal dynamics of communication.« less
  2. Human activity around the globe is a growing source of selection pressure on animal behavior and communication systems. Some animals can modify their vocalizations to avoid masking from anthropogenic noise. However, such modifications can also affect the salience of these vocalizations in functional contexts such as competition and mate choice. Such is the case in the well-studied Nuttall's white-crowned sparrow ( Zonotrichia leucophrys nuttalli ), which lives year-round in both urban San Francisco and nearby rural Point Reyes. A performance feature of this species' song is salient in territorial defense, such that higher performance songs elicit stronger responses in simulated territorial intrusions; but songs with lower performance values transmit better in anthropogenic noise. A key question then is whether vocal performance signals male quality and ability to obtain high quality territories in urban populations. We predicted white-crowned sparrows with higher vocal performance will be in better condition and will tend to hold territories with lower noise levels and more species-preferred landscape features. Because white-crowned sparrows are adapted to coastal scrub habitats, we expect high quality territories to contain lower and less dense canopies, less drought, more greenness, and more flat open ground for foraging. To test our predictions, we recordedmore »songs and measured vocal performance and body condition (scaled mass index and fat score) for a set of urban and rural birds ( N = 93), as well as ambient noise levels on their territories. Remote sensing metrics measured landscape features of territories, such as drought stress (NDWI), greenness (NDVI), mean canopy height, maximum height, leaf area density (understory and canopy), slope, and percent bare ground for a 50 m radius on each male territory. We did not find a correlation between body condition and performance but did find a relationship between noise levels and performance. Further, high performers held territories with lower canopies and less dense vegetation, which are species-preferred landscape features. These findings link together fundamental aspects of sexual selection in that habitat quality and the quality of sexually selected signals appear to be associated: males that have the highest performing songs are defending territories of the highest quality.« less
  3. 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 howmore »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« less
  4. 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, aremore »dependent on the complexity of the sensory scene.« less
  5. Investigation of the negative impacts of stress on reproduction has largely centered around the effects of the adrenal steroid hormone, corticosterone (CORT), and its influence on a system of tissues vital for reproduction—the hypothalamus of the brain, the pituitary gland, and the gonads (the HPG axis). Research on the action of CORT on the HPG axis has predominated the stress and reproductive biology literature, potentially overshadowing other influential mediators. To gain a more complete understanding of how elevated CORT affects transcriptomic activity of the HPG axis, we experimentally examined its role in male and female rock doves ( Columba livia ). We exogenously administrated CORT to mimic circulating levels during the stress response, specifically 30 min of restraint stress, an experimental paradigm known to increase circulating CORT in vertebrates. We examined all changes in transcription within each level of the HPG axis as compared to both restraint-stressed birds and vehicle-injected controls. We also investigated the differential transcriptomic response to CORT and restraint-stress in each sex. We report causal and sex-specific effects of CORT on the HPG transcriptomic stress response. Restraint stress caused 1567 genes to uniquely differentially express while elevated circulating CORT was responsible for the differential expression of 304 genes.more »Only 108 genes in females and 8 in males differentially expressed in subjects that underwent restraint stress and those who were given exogenous CORT. In response to elevated CORT and restraint-stress, both sexes shared the differential expression of 5 genes, KCNJ5 , CISH , PTGER3 , CEBPD , and ZBTB16 , all located in the pituitary. The known functions of these genes suggest potential influence of elevated CORT on immune function and prolactin synthesis. Gene expression unique to each sex indicated that elevated CORT affected more gene transcription in females than males (78 genes versus 3 genes, respectively). To our knowledge, this is the first study to isolate the role of CORT in HPG genomic transcription during a stress response. We present an extensive and openly accessible view of the role corticosterone in the HPG transcriptomic stress response. Because the HPG system is well conserved across vertebrates, these data have the potential to inspire new therapeutic strategies for reproductive dysregulation in multiple vertebrate systems, including our own.« less