Receiver psychology and the evolution of multicomponent signals

Many animals produce and respond to signals made up of multiple components. For example, many avian sexual displays are highly extravagant combinations of visual and acoustic elements, and are described as being 'multicomponent'. One possible reason for the evolution of such complex signals is that they provide more reliable information for receivers. However, receivers also influence signal evolution in another important way, by how they perceive and process signals: signallers will be selected to produce signals that are more easily received. The potential role of receiver psychology in the evolution of multicomponent signals has not previously been considered; in this review I present psychological results that support the notion that two components are better received than one alone. Detection can be improved by producing two components together, thus reducing the reaction time, increasing the probability of detection and lowering the intensity at which detection occurs. Discriminability of multicomponent stimuli is also made easier through better recognition, faster discrimination learning and multidimensional generalization. In addition, multicomponent stimuli also improve associative learning. I show that multicomponency does indeed improve signal reception in receivers, although the benefits of producing components in two sensory modalities (bimodal multicomponent signals) may be larger and more robust than producing them in just one (unimodal multicomponent signals). This highlights the need for consideration of receiver psychology in the evolution of multicomponent signals, and suggests that where signal components do not appear to be informative, they may instead be performing an important psychological function. Copyright 1999 The Association for the Study of Animal Behaviour.     

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.     

Spots and stripes: the evolution of repetition in visual signal form

It is common to find spatially repetitive patterns in animal visual signals. The evolution of such patterns is not well explained by existing theories of signal evolution. In this paper, we suggest that the evolution of signals with spatial repetition may be due to specific recognition problems and receiver biases. The logics of our hypotheses are studied in co-evolutionary simulations using artificial neural networks as models of receivers. These simulations yield repetitive visual signals under the following conditions: translations and reflections of the signal, partial obstruction of the signal, a fixed feature in the signal, and lateral inhibition in the receiver. In addition to regular repetitions our simulations sometimes result in other organisations of the signal such as blocky patterns and gradients.     

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.     

Resource value and the context dependence of receiver behaviour

Many animals use signals of fighting ability to minimize the costs of competition. Theory predicts that signals must be costly to remain reliable indicators of their bearer's abilities, but many signals of fighting ability lack obvious developmental costs. Instead, receivers are thought to maintain signal accuracy by behaving aggressively towards individuals with inaccurate signals (i.e. social costs). Models predict that the evolutionary stability of social cost signals depends on receivers trusting signals in certain contexts and testing signal accuracy in other contexts. Here, I use the signals of agonistic ability in Polistes dominulus wasps to provide the first experimental evidence that receiver responses to social cost signals are context dependent. During contests over low-value resources, wasps trust signals; they avoid patches of food guarded by rivals with elaborate signals. As the value of the resource increases, wasps become more likely to test signal accuracy. In fact, receivers challenge guards regardless of their signal phenotype when the resource is sufficiently valuable. Context-dependent receiver responses are likely to be an important behavioural mechanism underlying the evolution of social costs, as context-dependent responses allow receivers to minimize the costs of conflict while also ensuring signal accuracy.     

Environmental motion delays the detection of movement-based signals

Animal signals are constrained by the environment in which they are transmitted and the sensory systems of receivers. Detection of movement-based signals is particularly challenging against the background of wind-blown plants. The Australian lizard Amphibolurus muricatus has recently been shown to compensate for greater plant motion by prolonging the introductory tail-flicking component of its movement-based display. Here I demonstrate that such modifications to signal structure are useful because environmental motion lengthens the time lizard receivers take to detect tail flicks. The spatio-temporal properties of animal signals and environmental motion are thus sufficiently similar to make signal detection more difficult. Environmental motion, therefore, must have had an influence on the evolution of movement-based signals and motion detection mechanisms.     

Signal conflict in spider webs driven by predators and prey

Variation in the sensory physiologies of organisms can bias the receptions of signals, driving the direction of signal evolution. Sensory drive in the evolution of signals may be particularly important for organisms that confront trade-offs in signal design between the need for conspicuousness to allow effective transfer of information and the need for crypsis of the signal to unintended receivers. Several genera of orb-weaving spiders include conspicuous silk designs, stabilimenta, in the centre of their webs. Stabilimenta can be highly visible signals to predators, warning them of the presence of a noxious, sticky silk web. However, stabilimenta can also be used by prey as a signal in avoidance of webs, creating a trade-off in signal visibility. I argue that the derived spectral properties of stabilimentum silk have resulted in part from this conflict. The innate colour preferences of insects, their ability to learn colours, and the spectral properties of flowers all suggest that the reflectance spectra of stabilimenta renders them relatively cryptic to many insect prey, while maintaining their visibility to vertebrate predators.     

The evolution of signal form: effects of learned versus inherited recognition

Organisms can learn by individual experience to recognize relevant stimuli in the environment or they can genetically inherit this ability from their parents. Here, we ask how these two modes of acquisition affect signal evolution, focusing in particular on the exaggeration and cost of signals. We argue first, that faster learning by individual receivers cannot be a driving force for the evolution of exaggerated and costly signals unless signal senders are related or the same receiver and sender meet repeatedly. We argue instead that biases in receivers' recognition mechanisms can promote the evolution of costly exaggeration in signals. We provide support for this hypothesis by simulating coevolution between senders and receivers, using artificial neural networks as a model of receivers' recognition mechanisms. We analyse the joint effects of receiver biases, signal cost and mode of acquisition, investigating the circumstances under which learned recognition gives rise to more exaggerated signals than inherited recognition. We conclude the paper by discussing the relevance of our results to a number of biological scenarios.     

Do aggressive signals evolve towards higher reliability or lower costs of assessment?

It has been suggested that the evolution of signals must be a wasteful process for the signaller, aimed at the maximization of signal honesty. However, the reliability of communication depends not only on the costs paid by signallers but also on the costs paid by receivers during assessment, and less attention has been given to the interaction between these two types of costs during the evolution of signalling systems. A signaller and receiver may accept some level of signal dishonesty by choosing signals that are cheaper in terms of assessment but that are stabilized with less reliable mechanisms. I studied the potential trade‐off between signal reliability and the costs of signal assessment in the corncrake (Crex crex). I found that the birds prefer signals that are less costly regarding assessment rather than more reliable. Despite the fact that the fundamental frequency of calls was a strong predictor of male size, it was ignored by receivers unless they could directly compare signal variants. My data revealed a response advantage of costly signals when comparison between calls differing with fundamental frequencies is fast and straightforward, whereas cheap signalling is preferred in natural conditions. These data might improve our understanding of the influence of receivers on signal design because they support the hypothesis that fully honest signalling systems may be prone to dishonesty based on the effects of receiver costs and be replaced by signals that are cheaper in production and reception but more susceptible to cheating.     

Threshold assessment,categorical perception,and the evolution of reliable signaling

Animals often use assessment signals to communicate information about their quality to a variety of receivers, including potential mates, competitors, and predators. But what maintains reliable signaling and prevents signalers from signaling a better quality than they actually have? Previous work has shown that reliable signaling can be maintained if signalers pay fitness costs for signaling at different intensities and these costs are greater for lower quality individuals than higher quality ones. Models supporting this idea typically assume that continuous variation in signal intensity is perceived as such by receivers. In many organisms, however, receivers have threshold responses to signals, in which they respond to a signal if it is above a threshold value and do not respond if the signal is below the threshold value. Here, we use both analytical and individual-based models to investigate how such threshold responses affect the reliability of assessment signals. We show that reliable signaling systems can break down when receivers have an invariant threshold response, but reliable signaling can be rescued if there is variation among receivers in the location of their threshold boundary. Our models provide an important step toward understanding signal evolution when receivers have threshold responses to continuous signal variation.     

Error-proneness as a handicap signal

This paper describes two discrete signalling models in which the error-proneness of signals can serve as a handicap signal. In the first model, the direct handicap of sending a high-quality signal is not large enough to assure that a low-quality signaller will not send it. However, if the receiver sometimes mistakes a high-quality signal for a low-quality one, then there is an indirect handicap to sending a high-quality signal. The total handicap of sending such a signal may then still be such that a low-quality signaller would not want to send it. In the second model, there is no direct handicap of sending signals, so that nothing would seem to stop a signaller from always sending a high-quality signal. However, the receiver sometimes fails to detect signals, and this causes an indirect handicap of sending a high-quality signal that still stops the low-quality signaller of sending such a signal. The conditions for honesty are that the probability of an error of detection is higher for a high-quality than for a low-quality signal, and that the signaller who does not detect a signal adopts a response that is bad to the signaller. In both our models, we thus obtain the result that signal accuracy should not lie above a certain level in order for honest signalling to be possible. Moreover, we show that the maximal accuracy that can be achieved is higher the lower the degree of conflict between signaller and receiver. As well, we show that it is the conditions for honest signalling that may be constraining signal accuracy, rather than the signaller trying to make honest signals as effective as possible given receiver psychology, or the signaller adapting the accuracy of honest signals depending on his interests.     

Evolutionary novelty in communication between the sexes

The diversity of signalling traits within and across taxa is vast and striking, prompting us to consider how novelty evolves in the context of animal communication. Sexual selection contributes to diversification, and here we endeavour to understand the initial conditions that facilitate the maintenance or elimination of new sexual signals and receiver features. New sender and receiver variants can occur through mutation, plasticity, hybridization and cultural innovation, and the initial conditions of the sender, the receiver and the environment then dictate whether a novel cue becomes a signal. New features may arise in the sender, the receiver or both simultaneously. We contend that it may be easier than assumed to evolve new sexual signals because sexual signals may be arbitrary, sexual conflict is common and receivers are capable of perceiving much more of the world than just existing sexual signals. Additionally, changes in the signalling environment can approximate both signal and receiver changes through a change in transmission characteristics of a given environment or the use of new environments. The Anthropocene has led to wide-scale disruption of the environment and may thus generate opportunity to directly observe the evolution of new signals to address questions that are beyond the reach of phylogenetic approaches.     

Sensory trade-offs predict signal divergence in Surfperch

Unidirectional elaboration of male trait evolution (e.g., larger, brighter males) has been predicted by receiver bias models of sexual selection and empirically tested in a number of different taxa. This study identifies a bidirectional pattern of male trait evolution and suggests that a sensory constraint is driving this divergence. In this system, the inherent trade-off in dichromatic visual detection places limits on the direction that sensory biases may take and thus provides a quantitative test of the sensory drive model. Here I show that sensory systems with trade-offs in detection abilities produce bidirectional biases and that signal design properties match these biases. I combine species-specific measurements and ancestral estimates with visual detection modeling to examine biases in sensory and signaling traits across five fish species occupying optically diverse habitats in the Californian kelp forest. Species-specific divergence in visual pigments correlates with changes in environment and produces different sensory biases--favoring luminance (brightness) detection for some species and chromatic (color) detection for others. Divergence in male signals (spectral reflectance of orange, blue, and silver color elements) is predicted by each species' sensory bias: color divergence favors chromatic detection for species with chromatically biased visual systems, whereas species with luminance sensory biases have signals favoring luminance detection. This quantitative example of coevolution of communication traits varying in a bidirectional pattern governed by the environment is the first demonstration of sensory trade-offs driving signal evolution.     

Proportional processing of a visual mate choice signal in the green swordtail,Xiphophorus hellerii

During mate choice, receivers often assess the magnitude (duration, size, etc.) of signals that vary along a continuum and reflect variation in signaller quality. It is generally assumed that receivers assess this variation linearly, meaning each difference in signalling trait between signallers results in a commensurate change in receiver response. However, increasing evidence shows receivers can respond to signals non-linearly, for example through Weber's Law of proportional processing, where discrimination between stimuli is based on proportional, rather than absolute, differences in magnitude. We quantified mate preferences of female green swordtail fish, Xiphophorus hellerii, for pairs of males differing in body size. Preferences for larger males were better predicted by the proportional difference between males (proportional processing) than the absolute difference (linear processing). This demonstration of proportional processing of a visual signal implies that receiver perception may be an important mechanism selecting against the evolution of ever-larger signalling traits.     

THE EVOLUTION OF INDIVIDUAL VARIATION IN COMMUNICATION STRATEGIES

Communication is a process in which senders provide information via signals and receivers respond accordingly. This process relies on two coevolving conventions: a “sender code” that determines what kind of signal is to be sent given the sender's state; and a “receiver code” that determines the appropriate responses to different signal types. By means of a simple but generic model, we show that polymorphic sender and receiver strategies emerge naturally during the evolution of communication, and that the number of alternative strategies observed at equilibrium depends on the potential for error in signal production. Our model suggests that alternative communication strategies will evolve whenever senders possess imperfect information about their own quality or state, signals are costly, and genetic mechanisms allow for a correlation between sender and receiver behavior. These findings provide an explanation for recent reports of individual differences in communication strategies, and suggest that the amount of individual variation that can be expected in communication systems depends on the type of information being conveyed. Our model also suggests a link between communication and the evolution of animal personalities, which is that individual differences in the production and interpretation of signals can result in consistent differences in behavior.     

Conspicuousness is correlated with toxicity in marine opisthobranchs

Aposematism is defined as the use of conspicuous colouration to warn predators that an individual is chemically or otherwise defended. Mechanisms that drive the evolution of aposematism are complex. Theoretical and empirical studies show that conspicuousness can be either positively or negatively correlated with toxicity as once aposematism is established, species can allocate resources into becoming more conspicuous and/or increase secondary defences. Here, we investigated the evolution of conspicuousness and toxicity in marine opisthobranchs. Conspicuousness of colour signals was assessed using spectral reflectance measurements and theoretical vision models from the perspective of two reef fish signal receivers. The relative toxicity of chemicals extracted from each opisthobranch species was then determined using toxicity assays. Using a phylogenetic comparative analysis, we found a significant correlation between conspicuousness and toxicity, indicating that conspicuousness acts as an honest signal when signifying level of defence and provides evidence for aposematism in opisthobranchs.     

Attention-Seeking Displays

Animal communication abounds with extravagant displays. These signals are usually interpreted as costly signals of quality. However, there is another important function for these signals: to call the attention of the receiver to the signaller. While there is abundant empirical evidence to show the importance of this stage, it is not yet incorporated into standard signalling theory. Here I investigate a general model of signalling - based on a basic action-response game - that incorporates this searching stage. I show that giving attention-seeking displays and searching for them can be an ESS. This is a very general result and holds regardless whether only the high quality signallers or both high and low types give them. These signals need not be costly at the equilibrium and they need not be honest signals of any quality, as their function is not to signal quality but simply to call the attention of the potential receivers. These kind of displays are probably more common than their current weight in the literature would suggest.     

Phylogenetic tests of the sensory exploitation model of sexual selection

The diverse characteristics among closely related species are often involved in communication between the sexes. The traditional view that intersexual communication behaviors evolve in a complementary way is called into question by the sensory exploitation hypothesis. By predicting a lack of coordinated evolution between signals and preferences, the sensory exploitation hypothesis is distinct from other mechanisms of sexual selection. Tests of sensory exploitation have taken a multi-disciplinary approach, with insights from sensory physiology, behavior and phylogenetic comparisons. By demonstrating that signals and receivers are not closely coupled, and that signal preference pre-dates signal origin, proponents of the model argue that sensory exploitation is an evolutionary force responsible for the diversification of intersexual communication signals.     

Information,influence, and the causal-explanatory role of content in understanding receiver responses

Sceptics of informational terminology argue that by attributing content to signals, we fail to address nonhuman animal communication on its own terms. Primarily, we ignore that communication is sender driven: i.e. driven by the intrinsic physical properties of signals, themselves the result of selection pressures acting on signals to influence receivers in ways beneficial for senders. In contrast, information proponents argue that this ignores the degree to which communication is, in fact, receiver driven. The latter argue that an exclusive focus on the intrinsic mechanical properties of signals cannot explain why receivers respond as they do. This is because receivers are not prisoners of sender influence. They possess response flexibility, and so we can only explain why receivers respond to signals as they do by positing that receivers ‘derive information’ from signals. I argue that, while basically true, this response flexibility can take one of two forms depending on the causal-explanatory role of information in understanding the response of the receiver: diachronic, on the one hand; and synchronic, on the other. In species with diachronic response flexibility only, information is derived by receivers from signals in a minimal sense. In such cases, information is an ultimate explanatory construct: one underpinned by historical facts at the population level. Alternatively, in species with synchronic response flexibility, information is derived by receivers from signals in a richer sense. Here, information is a proximate explanatory construct: one underpinned by cognitive-mechanistic facts at the level of the individual organism. Without recognising the different ways information can be derived from signals, and the different causal-explanatory roles (ultimate vs proximate) information can play in understanding alternate kinds of receiver flexibility (diachronic vs synchronic), proponents of information leave themselves open to the charge of anthropomorphising some signalling systems.     

Male receiver bias for red agonistic signalling in a yellow-signalling widowbird: a field experiment

Receiver bias models of signal evolution are typically regarded as alternatives or complements to ornament evolution due to coevolving mate choice, whereas sexually or socially selected agonistic signals are rarely studied with respect to receiver psychology. Against the background of convergent evolution of red agonistic signals from yellow ancestors in the genus Euplectes (widowbirds and bishops), we experimentally test the function of a yellow signal in the montane marsh widowbird (E. psammocromius), as well as a hypothesized receiver bias for redder (longer wavelength) hues. In a field experiment in southern Tanzania, males that had their yellow wing patches blackened lost their territories or lost territorial contests more often than controls or reddened males, which together with a longer wavelength hue in territory holders, indicates an agonistic signal function. Males painted a novel red hue, matching that of red-signalling congeners, retained their territories and won contests more often than controls. To our knowledge, this is the first demonstration of a receiver bias driving agonistic signal evolution. Although the sensory or cognitive origin of this bias is yet unknown, it strengthens our view that genetically constrained signal production (i.e. carotenoid metabolism), rather than differential selection, explains the carotenoid colour diversification in Euplectes.