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.     

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.     

Dynamics of mimicry evolution

We simulated mimicry evolution by allowing three populations to cocvolvc: two populations of senders and one of receivers. Artificial neural networks were used to model receivers, and it was assumed that recognition was inherited. The senders' signals consisted of nine dimensions. Changes to receivers and senders were caused by random mutations during the course of the simulation. Whereas it paid both types of senders to elicit the same response from the receiver, it benefited the receiver to respond in this way only towards one of the sender types. The receiver was thus in conflict with one of the senders, e.g. as in Batesian mimicry. Monotonically increasing response gradients caused the appearance of the model and the mimic to move in the same direction. Mimicry evolved because the mimic approached the model faster than the model moved away. Even after mimicry was established the model and the mimic were constantly changing in appearance. Our results conform with what is known in comparative psychology and ethology about how animals respond to stimuli. Several of our results arc a direct consequence of recognition and have not, to our knowledge, been reported before, showing the importance of considering the recognition mechanism in detail when studying mimicry.     

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.     

Receiver bias for exaggerated signals in honeybees and its implications for the evolution of floral displays

Mechanistic models of animal signals posit the occurrence of biases on the part of receivers that could be potentially exploited by signallers. Such biases are most obvious when animals are confronted with exaggerated versions of signals they normally encounter. Signalling systems operating in plant-pollinator interactions are among the most highly coevolved, with plants using a variety of floral signals to attract pollinators. A number of observations suggest that pollinators preferentially visit larger floral displays although the benefit of this to either the plant or the pollinator is not always clear. We use a standard dual-choice experimental protocol to show that honeybees display a receiver bias for exaggerated size and colour contrast--two important components of floral signals--even when such signals do not indicate quality. We discuss the implications of this receiver bias for the evolution of floral displays and its possible exploitation by invading alien plants.     

Deception and the origin of honest signals

Deceptive signals are a challenge to explain because on average, signals should be reliable. When being deceived is costly to the receiver, a coevolutionary struggle between senders and receivers can ensue. Recent work by Macías Garcia and Ramirez raises the intriguing possibility that through such a coevolutionary process, cheats can become honest.     

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.     

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.     

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.     

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.     

Separating equilibria in continuous signalling games

Much of the literature on costly signalling theory concentrates on separating equilibria of continuous signalling games. At such equilibria, every signaller sends a distinct signal, and signal receivers are able to exactly infer the signaller's condition from the signal sent. In this paper, we introduce a vector-field solution method that simplifies the process of solving for separating equilibria. Using this approach, we show that continuous signalling games can have low-cost separating equilibria despite conflicting interests between signaller and receiver. We find that contrary to prior arguments, honesty does not require wasteful signals. Finally, we examine signalling games in which different signallers have different minimal-cost signals, and provide a mathematical justification for the argument that even non-signalling traits will be exaggerated beyond their phenotypic optimum when they are used by other individuals to judge condition or quality.     

Non-parallel coevolution of sender and receiver in the acoustic communication system of treefrogs

Advertisement calls of closely related species often differ in quantitative features such as the repetition rate of signal units. These differences are important in species recognition. Current models of signal-receiver coevolution predict two possible patterns in the evolution of the mechanism used by receivers to recognize the call: (i) classical sexual selection models (Fisher process, good genes/indirect benefits, direct benefits models) predict that close relatives use qualitatively similar signal recognition mechanisms tuned to different values of a call parameter; and (ii) receiver bias models (hidden preference, pre-existing bias models) predict that if different signal recognition mechanisms are used by sibling species, evidence of an ancestral mechanism will persist in the derived species, and evidence of a pre-existing bias will be detectable in the ancestral species. We describe qualitatively different call recognition mechanisms in sibling species of treefrogs. Whereas Hyla chrysoscelis uses pulse rate to recognize male calls, Hyla versicolor uses absolute measurements of pulse duration and interval duration. We found no evidence of either hidden preferences or pre-existing biases. The results are compared with similar data from katydids (Tettigonia sp.). In both taxa, the data are not adequately explained by current models of signal-receiver coevolution.     

Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish

The reproductive signals of two or more taxa may diverge in areas of sympatry, due to selection against costly reproductive interference. This divergence, termed reproductive character displacement (RCD), is expected in species-rich assemblages, where interspecific signal partitioning among closely related species is common. However, RCD is usually documented from simple two-taxon cases, via geographical tests for greater divergence of reproductive traits in sympatry than in allopatry. We propose a novel approach to recognizing and understanding RCD in multi-species communities--one that traces the displacement of signals within multivariate signal space during the ontogeny of individual animals. We argue that a case for RCD can be made if the amount of signal displacement between a pair of species after maturation is negatively correlated to distance in signal space before maturation. Our application of this approach, using a dataset of communication signals from a sympatric Amazonian assemblage of the electric fish genus Gymnotus, provides strong evidence for RCD among multiple species. We argue that RCD arose from the costs of heterospecific mismating, but interacted with sexual selection--favoring the evolution of conspicuous male signals that not only serve for mate-choice, but which simultaneously facilitate species recognition.     

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.     

CONSPIRATORIAL WHISPERS AND CONSPICUOUS DISPLAYS: GAMES OF SIGNAL DETECTION

Recent models of signaling have assumed that the expenditure required to ensure detection of a display is negligible and have concentrated instead on the costs that may be necessary to maintain honesty. Such models predict that individuals who share the same interests are likely to communicate using “conspiratorial whispers,” signals that are cheap and inconspicuous. Here, I present a game-theoretical model of signal detection (in a noisy environment, in the presence of potential eavesdroppers), which demonstrates that the idea of conspiratorial whispers is far too simplistic. It is true that in “cooperative” signaling systems (where signalers attempt to elicit responses that are beneficial for receivers), signal cost is not required to maintain honesty. However, some level of expenditure is still needed to ensure that a signal is reliably detected. Moreover, there exists a conflict of interest between signalers and receivers over the division of this expenditure. To predict the stable level of display in such cases, one needs to know how this conflict of interest will be resolved. The model reveals that the outcome may range from a whisper to a conspicuous and costly (though still conspiratorial) display. The more closely related the receiver is to the signaler, the greater the level of signal exaggeration that is expected—the opposite prediction to that of honest signaling models.     

Linking signal fidelity and the efficiency costs of communication

The handicap principle has been the overarching framework to explain the evolution and maintenance of communication. Yet, it is becoming apparent that strategic costs of signalling are not the only mechanism maintaining signal honesty. Rather, the fidelity of detecting signals can itself be strongly selected. Specifically, we argue that the fidelity of many signals will be constrained by the investment in signal generation and reception by the signaller and perceiver, respectively. Here, we model how investments in signal fidelity influence the emergence and stability of communication using a simple theoretical framework. The predictions of the model indicate that high‐cost communication can be stable whereas low‐cost intermediates are generally selected against. This dichotomy suggests that the most parsimonious route to the evolution of communication is for initial investment in communicative traits to be driven by noncommunicative functions. Such cues can appeal to pre‐existing perceptual biases and thereby stimulate signal evolution. We predict that signal evolution will vary between systems in ways that can be linked to the economics of communication to the two parties involved.     

How Does Individual Recognition Evolve? Comparing Responses to Identity Information in Polistes Species with and Without Individual Recognition

A wide range of complex social behaviors are facilitated by the recognition of individual conspecifics. Individual recognition requires sufficient phenotypic variation to provide identity information as well as receivers that process and respond to identity information. Understanding how a complex trait such as individual recognition evolves requires that we consider how each component has evolved. Previous comparative studies have examined phenotypic variability in senders and receiver learning abilities, although little work has compared receiver responses to identity information among related species with and without individual recognition. Here, we compare responses to identity information in two Polistes paper wasps: P. fuscatus, which visually recognizes individuals, and P. metricus, which does not normally show evidence of individual recognition. Although the species differ in individual recognition, the results of this study show that receiver responses to experimentally manipulated identity information are surprisingly similar in both species. Receivers direct less aggression toward identifiable individuals than unidentifiable individuals. Therefore, the responses necessary for individual recognition may pre‐date its evolution in the P. fuscatus lineage. Additionally, our data demonstrate the apparent binary differences in a complex behavior between the two species, such as individual recognition, likely involve incremental differences along a number of axes.     

The evolution of index signals to avoid the cost of dishonesty

Animals often convey useful information, despite a conflict of interest between the signaller and receiver. There are two major explanations for such ‘honest’ signalling, particularly when the size or intensity of signals reliably indicates the underlying quality of the signaller. Costly signalling theory (including the handicap principle) predicts that dishonest signals are too costly to fake, whereas the index hypothesis predicts that dishonest signals cannot be faked. Recent evidence of a highly conserved causal link between individual quality and signal growth appears to bolster the index hypothesis. However, it is not clear that this also diminishes costly signalling theory, as is often suggested. Here, by incorporating a mechanism of signal growth into costly signalling theory, we show that index signals can actually be favoured owing to the cost of dishonesty. We conclude that costly signalling theory provides the ultimate, adaptive rationale for honest signalling, whereas the index hypothesis describes one proximate (and potentially very general) mechanism for achieving honesty.     

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.     

Coevolution of senders and receivers of sexual signals: Genetic coupling and genetic correlations

The parallel evolution of senders and receivers of sexual signals has been a topic of research in both neuroethology and evolutionary quantitative genetics. Neuroethologists have debated whether the same physiological mechanism underlies both production and reception of a signal, and whether the same genes affect the physiology of communication in each sex. Quantitative geneticists have discussed the possibility that particular types of signals, and preferences for those types, are inherited together. Studies of communication by a variety of insect species do not provide strong support for a common physiological mechanism, but do not rule out the genetic effect. The neuroethological perspective may be of assistance in understanding the evolution of sexual communication because it offers a way to subdivide communication into units for genetic analysis.