Ripple effects in a communication network: anti-eavesdropper defence elicits elaborated sexual signals in rival males.

Emitting conspicuous signals into the environment to attract mates comes with the increased risk of interception by eavesdropping enemies. As a defence, a commonly described strategy is for signallers to group together in leks, diluting each individual's risk. Lekking systems are often highly social settings in which competing males dynamically alter their signalling behaviour to attract mates. Thus, signalling at the lek requires navigating fluctuations in risk, competition and reproductive opportunities. Here, we investigate how behavioural defence strategies directed at an eavesdropping enemy have cascading effects across the communication network. We investigated these behaviours in the túngara frog (Engystomops pustulosus), examining how a calling male's swatting defence directed at frog-biting midges indirectly affects the calling behaviour of his rival. We found that the rival responds to swat-induced water ripples by increasing his call rate and complexity. Then, performing phonotaxis experiments, we found that eavesdropping fringe-lipped bats (Trachops cirrhosus) do not exhibit a preference for a swatting male compared to his rival, but females strongly prefer the rival male. Defences to minimize attacks from eavesdroppers thus shift the mate competition landscape in favour of rival males. By modulating the attractiveness of signalling prey to female receivers, we posit that eavesdropping micropredators likely have an unappreciated impact on the ecology and evolution of sexual communication systems.

Tiny spies: mosquito antennae are sensitive sensors for eavesdropping on frog calls.

Most mosquito and midge species use hearing during acoustic mating behaviors. For frog-biting species, however, hearing plays an important role beyond mating as females rely on anuran calls to obtain blood meals. Despite the extensive work examining hearing in mosquito species that use sound in mating contexts, our understanding of how mosquitoes hear frog calls is limited. Here, we directly investigated the mechanisms underlying detection of frog calls by a mosquito species specialized on eavesdropping on anuran mating signals: Uranotaenia lowii. Behavioral, biomechanical and neurophysiological analyses revealed that the antenna of this frog-biting species can detect frog calls by relying on neural and mechanical responses comparable to those of non-frog-biting species. Our findings show that in Ur. lowii, contrary to most species, males do not use sound for mating, but females use hearing to locate their anuran host. We also show that the response of the antennae of this frog-biting species resembles that of the antenna of species that use hearing for mating. Finally, we discuss our data considering how mosquitoes may have evolved the ability to tap into the communication system of frogs.

Mixed-species assemblages and disease: the importance of differential vector and parasite attraction in transmission dynamics.

Individuals from multiple species often aggregate at resources, group to facilitate defense and foraging, or are brought together by human activity. While it is well-documented that host-seeking disease vectors and parasites show biases in their responses to cues from different hosts, the influence of mixed-species assemblages on disease dynamics has received limited attention. Here, we synthesize relevant research in host-specific vector and parasite bias. To better understand how vector and parasite biases influence infection, we provide a conceptual framework describing cue-oriented vector and parasite host-seeking behaviour as a two-stage process that encompasses attraction of these enemies to the assemblage and their choice of hosts once at the assemblage. We illustrate this framework, developing a case study of mixed-species frog assemblages, where frog-biting midges transmit trypanosomes. Finally, we present a mathematical model that investigates how host species composition and asymmetries in vector attraction modulate transmission dynamics in mixed-species assemblages. We argue that differential attraction of vectors by hosts can have important consequences for disease transmission within mixed-species assemblages, with implications for wildlife conservation and zoonotic disease. This article is part of the theme issue 'Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes'.

Tactics of evasion: strategies used by signallers to deter eavesdropping enemies from exploiting communication systems.

Eavesdropping predators, parasites and parasitoids exploit signals emitted by their prey and hosts for detection, assessment, localization and attack, and in the process impose strong selective pressures on the communication systems of the organisms they exploit. Signallers have evolved numerous anti-eavesdropper strategies to mitigate the trade-off between the costs imposed from signal exploitation and the need for conspecific communication. Eavesdropper strategies fall along a continuum from opportunistic to highly specialized, and the tightness of the eavesdropper-signaller relationship results in differential pressures on communication systems. A wide variety of anti-eavesdropper strategies mitigate the trade-off between eavesdropper exploitation and conspecific communication. Antagonistic selection from eavesdroppers can result in diverse outcomes including modulation of signalling displays, signal structure, and evolutionary loss or gain of a signal from a population. These strategies often result in reduced signal conspicuousness and in decreased signal ornamentation. Eavesdropping enemies, however, can also promote signal ornamentation. While less common, this alternative outcome offers a unique opportunity to dissect the factors that may lead to different evolutionary pathways. In addition, contrary to traditional assumptions, no sensory modality is completely 'safe' as eavesdroppers are ubiquitous and have a broad array of sensory filters that allow opportunity for signal exploitation. We discuss how anthropogenic change affects interactions between eavesdropping enemies and their victims as it rapidly modifies signalling environments and community composition. Drawing on diverse research from a range of taxa and sensory modalities, we synthesize current knowledge on anti-eavesdropper strategies, discuss challenges in this field and highlight fruitful new directions for future research. Ultimately, this review offers a conceptual framework to understand the diverse strategies used by signallers to communicate under the pressure imposed by their eavesdropping enemies.

Eavesdropping Micropredators as Dynamic Limiters of Sexual Signal Elaboration and Intrasexual Competition.

AbstractTo thoroughly understand the drivers of dynamic signal elaboration requires assessing the direct and indirect effects of naturally interacting factors. Here, we use structural equation modeling to test multivariate data from in situ observations of sexual signal production against a model of causal processes hypothesized to drive signal elaboration. We assess direct and indirect effects, and relative impacts, of male-male competition and attacks by eavesdropping frog-biting midges (Diptera: Corethrellidae) on call elaboration of male túngara frogs (Engystomops pustulosus). We find that the intensity of attacks by these micropredator flies drives the extent to which frogs elaborate their calls, likely due to a temporal trade-off between signaling and antimicropredator defense. Micropredator attacks appear to dynamically limit a male's call rate and complexity and consequently dampen the effects of intrasexual competition. In accounting for naturally interacting drivers of signal elaboration, this study presents a counterpoint to the mechanisms traditionally thought to drive sexual selection in this system. Moreover, the results shed light on the relatively unexamined and potentially influential role of eavesdropping micropredators in the evolution of sexual communication systems.

Dominance Can Increase Genetic Variance After a Population Bottleneck: A Synthesis of the Theoretical and Empirical Evidence.

Drastic reductions in population size, or population bottlenecks, can lead to a reduction in additive genetic variance and adaptive potential. Genetic variance for some quantitative genetic traits, however, can increase after a population reduction. Empirical evaluations of quantitative traits following experimental bottlenecks indicate that non-additive genetic effects, including both allelic dominance at a given locus and epistatic interactions among loci, may impact the additive variance contributed by alleles that ultimately influences phenotypic expression and fitness. The dramatic effects of bottlenecks on overall genetic diversity have been well studied, but relatively little is known about how dominance and demographic events like bottlenecks can impact additive genetic variance. Herein, we critically examine how the degree of dominance among alleles affects additive genetic variance after a bottleneck. We first review and synthesize studies that document the impact of empirical bottlenecks on dominance variance. We then extend earlier work by elaborating on 2 theoretical models that illustrate the relationship between dominance and the potential increase in additive genetic variance immediately following a bottleneck. Furthermore, we investigate the parameters that influence the maximum level of genetic variation (associated with adaptive potential) after a bottleneck, including the number of founding individuals. Finally, we validated our methods using forward-time population genetic simulations of loci with varying dominance and selection levels. The fate of non-additive genetic variation following bottlenecks could have important implications for conservation and management efforts in a wide variety of taxa, and our work should help contextualize future studies (e.g., epistatic variance) in population genomics.

Prey Exploits the Auditory Illusions of Eavesdropping Predators.

Mating signals have evolved to attract target receivers, even to the point of exploiting receivers through perceptual manipulation. Signals, however, can also expose signalers to nontarget receivers, including predators and parasites, and thus have also evolved to decrease enemy attraction. Here we show that male tree frogs (Smilisca sila) reduce their attractiveness to eavesdropping enemies (bats and midges) by overlapping their calls at near-perfect synchrony with the calls of neighboring conspecifics. By producing calls that closely follow those of other males, synchronizing S. sila take advantage of an auditory illusion where enemies are more attracted to the leading call. Female S. sila, however, are less susceptible to this illusion. Thus, synchronization among signaling males can result in acoustic crypsis from predators without affecting female attraction. Given the widespread use of conspicuous mating signals and eavesdropping enemies, perceptual exploitation of eavesdroppers is likely a common driver of signal evolution.

A new approach to improve acoustic trapping effectiveness for Aedes aegypti (Diptera: Culicidae).

Monitoring mosquito populations is essential to designing and implementing control strategies. Recent strategies based on releasing biologically modified mosquitoes have increased the need to effectively monitor mosquito abundance. Unfortunately, existing surveillance traps are of limited value due to their high cost and low capture rates. Here, we report the results of experiments designed to evaluate the effectiveness of an acoustic trap prototype. Stimuli synthesized from recordings of Ae. aegypti wingbeat signals and pure tones were evaluated as attractants to males in indoor and semi-field conditions. Overall, the acoustic trap´s efficacy differed significantly between indoor and semi-field conditions. After two hours of indoor recapture, ∼69% of males were collected from acoustic traps broadcasting pure tones while ∼78% of males were collected using synthesized wingbeat signals. Under semi-field conditions, however, acoustic traps collected less than ∼1.7% of the males released. Increasing the intensity of the signals up to 90 dB (SPL re. 20 uPa at 1 m from the trap) did not improve the capture rate under semi-field conditions. Overall, our results indicate that acoustic signals synthesized from recordings of wingbeats can be used to enhance capture of male Ae. aegypti.

Laryngeal Demasculinization in Wild Cane Toads Varies with Land Use.

Anthropogenic factors, including the spread of endocrine-disrupting chemicals, have been linked to alterations in the reproductive physiology, morphology, and behavior of wildlife. Few studies of endocrine disruption, however, focus on secondary sexual traits that affect mating signals, despite their importance for reproductive success. The larynx of many anurans (frogs and toads), for example, is larger in males than in females and is crucial for producing mating calls. We aim to determine if wild populations of cane toads (Rhinella marina) near sugarcane fields in Florida have demasculinized larynges when compared to populations near urban areas. We find evidence of demasculinization in both primary and secondary sexual traits in male toads living near sugarcane. Relative to body size, the laryngeal mass, vocal cord length, and dilator muscle width are all reduced in males from sugarcane regions compared to their urban counterparts. Strong correlations between primary and secondary male sexual traits indicate that demasculinization occurs in concert both within and across diverse organs, including the testes, larynx, and skin. Our results show that anurans near sugarcane fields have demasculinized reproductive systems, that this disruption extends to secondary sexual traits like the larynx, and that it is likely due to anthropogenic causes.

Synchronized mating signals in a communication network: the challenge of avoiding predators while attracting mates.

Conspicuous mating signals attract mates but also expose signallers to predators and parasites. Signal evolution, therefore, is driven by conflicting selective pressures from multiple receivers, both target and non-target. Synchronization of mating signals, for example, is an evolutionary puzzle, given the assumed high cost of reduced female attraction when signals overlap. Synchronization may be beneficial, however, if overlapping signals reduce attraction of non-target receivers. We investigate how signal synchronization is shaped by the trade-off between natural and sexual selection in two anuran species: pug-nosed tree frogs (Smilisca sila), in which males produce mating calls in near-perfect synchrony, and túngara frogs (Engystomops pustulosus), in which males alternate their calls. To examine the trade-off imposed by signal synchronization, we conducted field and laboratory playback experiments on eavesdropping enemies (bats and midges) and target receivers (female frogs). Our results suggest that, while synchronization can be a general strategy for signallers to reduce their exposure to eavesdroppers, relaxed selection by females for unsynchronized calls is key to the evolution and maintenance of signal synchrony. This study highlights the role of relaxed selection in our understanding of the origin of mating signals and displays.

The Cognitive Ecology of Stimulus Ambiguity: A Predator-Prey Perspective.

Organisms face the cognitive challenge of making decisions based on imperfect information. Predators and prey, in particular, are confronted with ambiguous stimuli when foraging and avoiding attacks. These challenges are accentuated by variation imposed by environmental, physiological, and cognitive factors. While the cognitive factors influencing perceived ambiguity are often assumed to be fixed, contemporary findings reveal that perceived ambiguity is instead the dynamic outcome of interactive cognitive processes. Here, we present a framework that integrates recent advances in neurophysiology and sensory ecology with a classic decision-making model, signal detection theory (SDT), to understand the cognitive mechanisms that shape perceived stimulus ambiguity in predators and prey. Since stimulus ambiguity is pervasive, the framework discussed here provides insights that extend into nonforaging contexts.

Nineteen Years of Consistently Positive and Strong Female Mate Preferences despite Individual Variation.

Sexual selection driven by mate choice has generated some of the most astounding diversity in nature, suggesting that population-level preferences should be strong and consistent over many generations. On the other hand, mating preferences are among the least repeatable components of an individual animal's phenotype, suggesting that consistency should be low across an animal's lifetime. Despite decades of intensive study of sexual selection, there is almost no information about the strength and consistency of preferences across many years. In this study, we present the results of more than 5,000 mate choice tests with a species of wild frog conducted over 19 consecutive years. Results show that preferences are positive and strong and vary little across years. This consistency occurs despite the fact that there are substantial differences among females in their strength of preference. We also suggest that mate preferences in populations that are primarily the result of sensory exploitation might be more stable over time than preferences that are primarily involved in assessing male quality.

Adaptive changes in sexual signalling in response to urbanization.

Urbanization can cause species to adjust their sexual displays, because the effectiveness of mating signals is influenced by environmental conditions. Despite many examples that show that mating signals in urban conditions differ from those in rural conditions, we do not know whether these differences provide a combined reproductive and survival benefit to the urban phenotype. Here we show that male túngara frogs have increased the conspicuousness of their calls, which is under strong sexual and natural selection by signal receivers, as an adaptive response to city life. The urban phenotype consequently attracts more females than the forest phenotype, while avoiding the costs that are imposed by eavesdropping bats and midges, which we show are rare in urban areas. Finally, we show in a translocation experiment that urban frogs can reduce risk of predation and parasitism when moved to the forest, but that forest frogs do not increase their sexual attractiveness when moved to the city. Our findings thus reveal that urbanization can rapidly drive adaptive signal change via changes in both natural and sexual selection pressures.

A new species of frog-biting midge from Papua New Guinea with a key to the described Corethrellidae of the Australopapuan region (Diptera, Corethrellidae, Corethrella).

Corethrellaoppositophila Kvifte & Bernal, sp. n. is described based on one male and six female specimens collected at 2200 m a.s.l. on Mount Wilhelm, Papua New Guinea. The species is the fourth species of frog-biting midge described from this country and appears similar to Corethrellasolomonis Belkin based on pigmentation of legs and abdominal tergites. It differs from C.solomonis, however, in the shape of female flagellomeres I-III, and in the thorax which has a dark brown vertical stripe. The new species is named for its sexually dimorphic flagellomeres, which are short and squat in the female and elongate in the male. These differences in morphological characters are discussed in light of the likely sexual differences in functional uses of the antennae, as males use them for mating only whereas females use them both for mating and prey location. An emended key is presented to the described Australopapuan species of Corethrellidae.

Anuran predators overcome visual illusion: dazzle coloration does not protect moving prey.

Predators everywhere impose strong selection pressures on the morphology and behavior of their prey, but the resulting antipredator adaptations vary greatly among species. Studies of adaptive coloration in prey species have generally focused on cryptic or aposematic prey, with little consideration of color patterns in palatable mobile prey. Complex color patterns have been proposed to decrease the ability of visual predators to capture moving prey (motion dazzle effect). Most support for this hypothesis, however, comes from experiments with human subjects and simulated prey. We tested the motion dazzle effect using, for the first time, natural predators (cane toads, Rhinella marina) and live prey (house crickets, Acheta domesticus) with altered color patterns. We found no support for the motion dazzle effect as striped crickets did not fare better than solid colored ones. Crickets that spent more time moving, however, were more likely to be eaten. Our results suggest that motion specialized visual predators such as toads overcome the motion dazzle effect and impose stronger selection pressure on prey behavior than on coloration. These findings emphasize the importance of sensory specializations of predators in mediating antipredator strategies.

Exploratory behavior of a native anuran species with high invasive potential.

Exploratory behavior can be a key component of survival in novel or changing environments, ultimately determining population establishment. While many studies have investigated the behavior of wild animals in response to novel food items or objects, our understanding of how they explore novel environments is limited. Here, we examine how experience affects the foraging behavior of a species with high invasive potential. In particular, we investigate the movement and behavior of cane toads as a function of experience in a novel environment, and how the presence of food modulates exploration. Cane toads, from a population in their native range, were repeatedly tested in a large, naturalistic arena with or without food present. Both groups exhibited significant but different changes in exploratory behavior. While toads in an environment without food reduced exploratory behavior over trials, those with food present increased both food intake per trial and the directness of their paths to food, resulting in fewer approaches to food patches over time. Our results suggest that cane toads learn patch location and provide preliminary evidence suggesting toads use spatial memory, not associative learning, to locate food. In sum, we show that with experience, cane toads alter their behavior to increase foraging efficiency. This study emphasizes the role of learning in foraging in cane toads, a characteristic that may have facilitated their success as invaders.