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 on visual secrets

Private communication may benefit signalers by reducing the costs imposed by potential eavesdroppers such as parasites, predators, prey, or rivals. It is likely that private communication channels are influenced by the evolution of signalers, intended receivers, and potential eavesdroppers, but most studies only examine how private communication benefits signalers. Here, we address this shortcoming by examining visual private communication from a potential eavesdropper’s perspective. Specifically, we ask if a signaler would face fitness consequences if a potential eavesdropper could detect its signal more clearly. By integrating studies on private communication with those on the evolution of vision, we suggest that published studies find few taxon-based constraints that could keep potential eavesdroppers from detecting most hypothesized forms of visual private communication. However, we find that private signals may persist over evolutionary time if the benefits of detecting a particular signal do not outweigh the functional costs a potential eavesdropper would suffer from evolving the ability to detect it. We also suggest that all undetectable signals are not necessarily private signals: potential eavesdroppers may not benefit from detecting a signal if it co-occurs with signals in other more detectable sensory modalities. In future work, we suggest that researchers consider how the evolution of potential eavesdroppers’ sensory systems influences private communication. Specifically, we suggest that examining the fitness correlates and evolution of potential eavesdroppers can help (1) determine the likelihood that private communication channels are stable over evolutionary time, and (2) demonstrate that undetectable signals are private signals by showing that signalers benefit from a reduction in detection by potential eavesdroppers.     

Sexual Signals as Advertisers of Resistance to Mistakes

To be evolutionarily stable, sexual signals need to convey information regarding the quality or motivation of individuals. This can be achieved through direct or indirect signal costs that guarantee honest communication or through signal designs that facilitate the assessment of quality. Here, I present the case for an alternative hypothesis: that signalling exposes informative mistakes. Signalling mistakes range from occasional to frequent and from slight distortions of typical signals to grossly atypical signals. Their occurrence may be enhanced by disease or stress, thus revealing individual quality or motivation, and receivers typically respond negatively to them. By this mechanism, honest communication is due to costs of developing resistance to mistakes. Therefore, the hypothesis can function independently of signal design costs, although it can also be enhanced by signal design costs when those increase the occurrence of mistakes. This hypothesis widens the scope of signals expected to be sexually selected and creates new approaches to research in sexual selection and animal communication.     

Timing actions to avoid refractoriness: a simple solution for streaming sensory signals

Segmenting self- from allo-generated signals is crucial for active sensory processing. We report a dynamic filter used by South American pulse electric fish to distinguish active electro-sensory signals carried by their own electric discharges from other concomitant electrical stimuli (i.e. communication signals). The filter has a sensory component, consisting of an onset type central electro-sensory neuron, and a motor component, consisting of a change in the fish's discharge rate when allo-generated electrical events occur in temporal proximity to the fish's own discharge. We investigated the sensory component of the filter by in vitro mimicking synaptic inputs occurring during behavioral responses to allo-generated interfering signals. We found that active control of the discharge enhances self-generated over allo-generated responses by forcing allo-generated signals into a central refractory period. This hypothesis was confirmed by field potential recordings in freely discharging fish. Similar sensory-motor mechanisms may also contribute to signal segmentation in other sensory systems.     

Issues in the classification of multimodal communication signals

Communication involves complex behavior in multiple sensory channels, or "modalities." We provide an overview of multimodal communication and its costs and benefits, place examples of signals and displays from an array of taxa, sensory systems, and functions into our signal classification system, and consider issues surrounding the categorization of multimodal signals. The broadest level of classification is between signals with redundant and nonredundant components, with finer distinctions in each category. We recommend that researchers gather information on responses to each component of a multimodal signal as well as the response to the signal as a whole. We discuss the choice of categories, whether to categorize signals on the basis of the signal or the response, and how to classify signals if data are missing. The choice of behavioral assay may influence the outcome, as may the context of the communicative event. We also consider similarities and differences between multimodal and unimodal composite signals and signals that are sequentially, rather than simultaneously, multimodal.     

Habitat-specific sensory-exploitative signals in birds: propensity of dipteran prey to cause evolution of plumage variation in flush-pursuit insectivores

Sensory exploitation occurs when signals trigger behavioral reactions that diminish the receiver's fitness. Research in this area focuses on the match between the signal's form and the receiver's sensitivity, but the effect of habitat on interspecific sensory exploitation is rarely addressed. Myioborus redstarts use conspicuous wing and tail displays of contrasting black-and-white plumage patches to flush dipteran insects, which are then pursued and captured in flight. Previous studies have shown that by increasing the distance at which insects perform an escape response, conspicuous visual displays improve the birds' foraging performance. We tested the hypothesis that selection for a visual signal that maximizes prey escape distance under local habitat conditions can lead to the evolution of geographic variation in plumage pattern among Myioborus redstarts. Using models of foraging birds, we recorded the escape responses of Dipterous insects to a range of plumage patterns and background tones (from light to dark) to determine whether the plumage pattern that maximizes prey flushing is dependent upon that habitat (background) against which birds are viewed by their prey. Our results indicate that the effectiveness of a particular plumage pattern in flushing dipteran prey depends strongly on the background against which that plumage pattern is displayed, and darker habitat (background) conditions generally favor plumages with more extensive patches of white in the tail. However, the addition of white wing patches that imitate the plumage of the painted redstart (Myioborus pictus) generally increases insect escape responses but reduces the effect that tail pattern variation and background tone have on escape behavior. These experiments support the hypothesis that habitat-specific natural selection to enhance sensory exploitation of prey escape responses could produce geographic variation in plumage patterns of flush-pursuers.     

The Acoustic Properties of Low Intensity Vocalizations Match Hearing Sensitivity in the Webbed-Toed Gecko,Gekko subpalmatus

The design of acoustic signals and hearing sensitivity in socially communicating species would normally be expected to closely match in order to minimize signal degradation and attenuation during signal propagation. Nevertheless, other factors such as sensory biases as well as morphological and physiological constraints may affect strict correspondence between signal features and hearing sensitivity. Thus study of the relationships between sender and receiver characteristics in species utilizing acoustic communication can provide information about how acoustic communication systems evolve. The genus Gekko includes species emitting high-amplitude vocalizations for long-range communication (loud callers) as well as species producing only low-amplitude vocalizations when in close contact with conspecifics (quiet callers) which have rarely been investigated. In order to investigate relationships between auditory physiology and the frequency characteristics of acoustic signals in a quiet caller, Gekko subpalmatus we measured the subjects’ vocal signal characteristics as well as auditory brainstem responses (ABRs) to assess auditory sensitivity. The results show that G. subpalmatus males emit low amplitude calls when encountering females, ranging in dominant frequency from 2.47 to 4.17 kHz with an average at 3.35 kHz. The auditory range with highest sensitivity closely matches the dominant frequency of the vocalizations. This correspondence is consistent with the notion that quiet and loud calling species are under similar selection pressures for matching auditory sensitivity with spectral characteristics of vocalizations.     

How to cheat when you cannot lie? Deceit pollination in Begonia gracilis

Mimicry between rewarding and non-rewarding flowers within individuals has been accepted as a strategy favored by selection to deceive pollinators. It has been proposed that this mechanism relies on the exploitation of pollinator's sensory biases, but field evidence is still scarce. In this study, we describe the mechanism of deceit pollination in the monoecious herb Begonia gracilis, a species with exposed rewarding structures (pollen) and intersexual mimicry. Specifically, we test the role of mimicry and exploitation of sensory biases on the reproductive success of male (pollination visitation) and female flowers (probability of setting fruits). We show that pollinators' perception of the amount of reward provided by male flowers is influenced by the independent variation in the sizes of the androecium and the perianth. Large rewarding structures and small perianths were preferred by pollinators, suggesting a central role of the relative size of the rewarding structure on pollinators' foraging decisions. Hence, rewarding male flowers cheat pollinators by exploiting their sensory biases, a strategy followed by non-rewarding female flowers. We suggest that intersexual mimicry operates through the functional resemblance of male flowers' deceit strategy. Artificial manipulation of the flowers supports our findings in natural conditions. Overall, we propose that the continuous and independent variation in the size of the perianth and the reproductive organs among male and female flowers could itself be adaptive.     

Economic models of animal communication

Many models of animal signal evolution fail to incorporate an explicit strategy for receivers prior to the evolution of signals. When reasonable assumptions are made for such strategies, we have shown that there is a minimal accuracy of signal coding that is required before receivers should attend to signals (Bradbury & Vehrencamp 1998, Principles of Animal Communication). Depending upon the relative payoffs of correct and incorrect decisions by receivers, this minimal accuracy can be quite high. Here we use this result to explain why so many signals appear to be traits that provided useful information to receivers before becoming ritualized into signals. Our model also supports one prediction of sensory drive models: that latent preferences may selectively favour some signal precursors over others. However, it imposes a serious constraint on sensory drive by requiring that there be sufficient benefits to a receiver to compensate for the costs of disrupting the optimal receiver strategy used before exploitation. Finally, we discuss the overlap between signal honesty and accuracy and show how senders that completely disagree with receivers about appropriate receiver decisions may still benefit by providing moderately honest and accurate signals. Copyright 2000 The Association for the Study of Animal Behaviour.     

A test of sensory exploitation in the swordtail characin (Corynopoma riisei) based on colour matching between female prey and a male ornament

The sensory exploitation hypothesis states that pre-existing biases in female sensory systems may generate strong selection on male signals to match such biases. As environmental conditions differ between populations, sexual preferences resulting from natural selection are expected to vary as well. The swordtail characin (Corynopoma riisei) is a species in which males carry a flag-like ornament growing from the operculum that has been proposed to function as a prey mimic to attract females. Here, we investigated if female plasticity in feeding preferences is associated with plasticity in preference for an artificial male ornament in this species. Females were trained for 10 days by offering them differently coloured food items and were then tested for changes in preferences for differently coloured artificial male ornaments according to foraging experience. We found a rapid and pronounced change in female preference for the colouration of the artificial ornament according to food training. Thus our results support the possibility that sensory exploitation may act as a driving force for female preferences for male ornaments in this species.     

Multimodal Signaling in Male and Female Foot-Flagging Frogs Staurois guttatus (Ranidae): An Alerting Function of Calling

In multimodal communication, individuals use several sensory modalities for information transfer. We report on novel observations of foot‐flagging in the Bornean ranid frog Staurois guttatus that is temporally linked to advertisement calling. In addition, we document the first case of foot‐flagging in a female anuran as well as additional visual displays in both males and females including arm‐waving, vocal‐sac pumping and open‐mouth display. In males, advertisement calls and foot‐flags were given throughout most of the day, suggesting that acoustic and visual signals form a multicomponent and multimodal display. We tested the efficacy‐based alerting signal hypothesis of multimodal communication using acoustic playback experiments with males. This hypothesis predicts that an initial signal draws the receiver's attention to the location of a subsequent more informative signal. Several lines of evidence supported the alerting hypothesis. First, the latency between foot‐flags and advertisement calls was significantly higher than that between advertisement calls and foot‐flags, suggesting a functional linkage with calls drawing attention to foot‐flags. Secondly, advertisement calling had a signaling function with males responding significantly more often with both calls and foot‐flags compared with pre‐ and post‐playback control periods. Finally, and most notably, all males tested turned towards the playback stimulus, suggesting that the advertisement call serves to focus their attention on subsequent signals. We discuss the potential of multimodal signaling for conspecific and heterospecific communication and the circumstances under which such a multimodal communication system could evolve.     

Biases in signal evolution: learning makes a difference

It is now well established that signal receivers have a key role in the evolution of animal communication: the suite of sensory and cognitive processes by which animals perceive and learn about their environment can have a significant impact on signal design. A crucial property of these information-processing mechanisms is the emergence of 'receiver bias' in the behavioural responses to signals. Whereas most research has focussed on receiver biases in the sensory system, more recent studies show that biases can also arise from learning about signals. Here, we highlight how learning-based biases can arise, and how these differ from biases emerging from sensory systems in their impact on signal evolution.     

Coevolution of visual signals and eye morphology in Polistes paper wasps

To be effective, signals must propagate through the environment and be detected by receivers. As a result, signal form evolves in response to both the constraints imposed by the transmission environment and receiver perceptual abilities. Little work has examined the extent to which signals may act as selective forces on receiver sensory systems to improve the efficacy of communication. If receivers benefit from accurate signal assessment, selection could favour sensory organs that improve discrimination of established signals. Here, we provide evidence that visual resolution coevolves with visual signals in Polistes wasps. Multiple Polistes species have variable facial patterns that function as social signals, whereas other species lack visual signals. Analysis of 19 Polistes species shows that maximum eye facet size is positively associated with both eye size and presence of visual signals. Relatively larger facets within the eye''s acute zone improve resolution of small images, such as wasp facial signals. Therefore, sensory systems may evolve to optimize signal assessment. Sensory adaptations to facilitate signal detection may represent an overlooked area of the evolution of animal communication.     

Palomena prasina (Hemiptera: Pentatomidae) vibratory signals and their tuning with plant substrates

Palomena prasina is interesting for the study of vibrational communication within the Pentatomid subfamily Pentatominae, because its host range is limited to woody plants, unlike the better known Nezara viridula, whose vibrational communication is commonly used as a model for the whole family. The vibrational repertoire of P. prasina was described several decades ago and is redescribed in this paper using modern methods for non-contact vibration recording. Additionally, we hypothesized that this species has retained the capacity for signal frequency variation necessary for tuning to resonance properties of various host plants of Pentatominae, but if the signals are emited in the absence of mechanical feedback, they are tuned more specifically to their native acoustic environment — woody plants. By recording live bugs signalling on different substrates and comparing spectral properties of their signals among substrates, we found that there is a match between the signals emitted on a woody branch and those emitted on a non-resonant surface, while spectral properties of signals emitted on herbaceous plants differ. Our findings provide evidence in support of the signal tuning hypothesis and shed further light on the crucial role of substrate in vibrational communication of insects.     

How sensory drive can promote speciation

Some of the most spectacular and diverse traits in animals are the signals used to attract mates. Closely related species often differ dramatically in signaling traits, in spite of similarity in other morphological traits. The idea that reproductive isolation arises when male mating signals and female preferences differ among populations is an old one. However, until recently, there was almost no information on what generates diversity in mating signals and preferences. This is beginning to change, with emerging results that highlight the importance of habitat differences in generating this diversity. Such differences in ecology are at the root of one hypothesis for divergence in sexual signaling – sensory drive. The sensory drive hypothesis focuses on how communication systems adapt to local environments and predicts that divergence in communication systems will occur when environments differ. Reproductive isolation can arise as a byproduct of this adaptive divergence in behavior.     

Negative Association Between Conspicuous Visual Display and Chemosensory Behavior in Two Phrynosomatid Lizards

Communication in one sensory modality can influence communication in others. Lizards in many phrynosomatid species use primarily visual but also chemical signals. The striped plateau lizard, Sceloporus virgatus , exhibits evolutionary loss of a male color signal that in many species is used during aggressive postural displays towards conspecific males. These patches are used similarly in Urosaurus , the sister genus to Sceloporus . We compared a species in which a color signal has been lost, S. virgatus , to a species retaining the ancestral character state of blue abdominal display patches, Urosaurus ornatus , the common tree lizard, to test two hypotheses: (i) conspicuous postural displays that reveal the abdominal patch location are used less in the species that has lost the color patches; and (ii) potential chemical signals are used more in the species with the color loss. We analyzed both visual display behavior (push-up, full-show) and chemosensory behavior (tongue flick and nose tap) of male lizards following their introduction to a resident conspecific male in his home terrarium. Resident males performed very low rates of all behaviors, but intruders exhibited sufficient behavior for analysis.
Supporting the first hypothesis, S. virgatus were less likely than U. ornatus to perform full-show, a display that reveals abdominal skin. Male S. virgatus were more likely to perform push-up than U. ornatus , although S. virgatus performed push-up infrequently. Push-up is a postural display that does not specifically reveal the abdominal patch location. Supporting the second hypothesis, S . virgatus were more likely to perform chemosensory behaviors and performed them at a greater rate than did U. ornatus . Work comparing more closely related species is warranted to determine whether a negative association between conspicuous visual displays and chemosensory behavior is a general pattern.     

The evolution of birdsong on islands

Islands are simplified, isolated ecosystems, providing an ideal set‐up to study evolution. Among several traits that are expected to change on islands, an interesting but poorly understood example concerns signals used in animal communication. Islands are typified by reduced species diversity, increased population density, and reduced mate competition, all of which could affect communication signals. We used birdsong to investigate whether there are systematic changes in communication signals on islands, by undertaking a broad comparison based on pairs of closely related island‐mainland species across the globe. We studied song traits related to complexity (number of different syllables, frequency bandwidth), to vocal performance (syllable delivery rate, song duration), and also three particular song elements (rattles, buzzes, and trills) generally implicated in aggressive communication. We also investigated whether song complexity was related to the number of similar sympatric species. We found that island species were less likely to produce broadband and likely aggressive song elements (rattles and buzzes). By contrast, various aspects of song complexity and performance did not differ between island and mainland species. Species with fewer same‐family sympatric species used wider frequency bandwidths, as predicted by the character release hypothesis, both on continents and on islands. Our study supports the hypothesis of a reduction in aggressive behavior on islands and suggests that discrimination against closely related species is an important factor influencing birdsong evolution.     

Why some rails have white tails: the evolution of white undertail plumage and anti-predator signaling

Conspicuous plumage patches have evolved in birds as conspecific signals for mate attraction and assessment, intersexual competition or to signal alarm. Signals may alternatively be directed at potential predators to discourage pursuit. Rails (Family Rallidae) are ground-dwelling birds, many of which inhabit wetlands, while others occur in forests and grasslands. They are renown for their secretive nature and the tendency to flick their tails when observed. This behavior is more conspicuous in species with white undertail coverts that contrast sharply with darker body plumage. Using species comparisons and controlling for phylogeny, we investigated four hypotheses for the evolution of white undertail coverts in rails. We found little support for the hypothesis that white tails are sexually selected: white tails were not more common in species with polygamous as opposed to monogamous mating systems, species with sexual dimorphism, nor species that display their tails in courtship. Nor did our results support the hypothesis that white tail plumage evolved for intersexual competition during territorial interactions. Instead, we found that species that flock for at least part of the year and species found in open as opposed to concealing habitats were significantly more likely to have white undertail coverts. Rail species inhabiting concealing habitats are less commonly gregarious and more likely selected for crypsis. Using phylogenetically-controlled statistical inference we found that adaptation to open wetland habitats significantly precedes the evolution of white undertails, whereas gregariousness likely evolved later in some lineages. The inferred order of trait evolution suggests that this plumage characteristic could have been selected primarily for enhancement of an anti-predator signal rather than a social signal for conspecifics.     

Species‐specific communication bars interspecific mating between syntopic species of Zwicknia stoneflies (Plecoptera: Capniidae)

Most Northern Hemisphere stoneflies have species‐specific mating signals that are generally thought to constitute a barrier against interspecific mating. We tested this hypothesis in two species of the genus Zwicknia that have only very recently been recognised as distinct species, and that were found to occur together in a stream in Lower Saxony, Germany. Analyses of molecular markers COI and 28S in combination with wing length (distinguishing males of both species) and mating signals revealed no instance of hybridisation among 23 studied specimens. In addition, eleven further males identified on the basis of morphology alone all produced the expected species‐specific signal. Females and males of both species were presented with played back conspecific and heterospecific signals and duetting sequences, and responded only to conspecific stimuli. This lends support to the hypothesis that the intersexual communication system functions as an important pre‐mating barrier against gene flow, although post‐mating isolation cannot be excluded. Interspecific mating did occur when a mixed pair was confined together in a small container. Males of both species were found to call in response to played back duetting sequences with stereotypic latencies that are clearly longer than the latencies in male‐female duets. We interpret this as an indication of eavesdropping behaviour coupled with attempts to take over the perceived duet. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 969–980.