Primate Communication: By Nature Honest, or by Experience Wise?

We review evolutionary views on honesty and deception and their application to studies of nonhuman primate communication. There is evidence that some primate signals are likely to be accurate on the basis of costliness. They appear most often in contexts that include overtly competitive interactions in which unrelated individuals have limited access to information about one another. However, both game theoretic models and most empirical work suggest that costly signals are not often likely to be the basis for honest communication in nonhuman primates. Inexpensive signaling can exist in contexts wherein communication occurs among related animals, something common among many nonhuman primate societies. Another condition in which inexpensive signaling is possible and that is also typical of nonhuman primates, is when sender and receiver both benefit from coordinated interactions. Additionally, when individuals interact repeatedly and can use past interactions to assess the honesty of signals and to modify future response to signals, low-cost signals can evolve. Nonhuman primates appear to deal with the problem of deception via skeptical responding, which can be largely accounted for by learning rules and the fact that they live in stable social groups and can recognize one another and recall past interactions.     

Depression and suicidality as evolved credible signals of need in social conflicts

Mental health professionals generally view major depression and suicidality as pathological responses to stress that elicit aversive responses from others. An alternative hypothesis grounded in evolutionary theory contends that depression and suicidality are honest signals of need in response to adversity that can increase support from reluctant others when there are conflicts of interest. To test this hypothesis, we examined responses to emotional signals in a preregistered experimental vignette study involving claims of substantial need in the presence of conflicts of interest and private information about the signaler's true level of need. In a sample of 1240 participants recruited from Amazon Mechanical Turk, costlier signals like depression and suicidality increased perceptions of need, reduced perceptions of manipulativeness, and increased likelihood of support compared to simple verbal requests and crying without further symptoms. The effect of signaling on likelihood of support was largely mediated by the effect of signaling on participants' belief that the signaler was genuinely in need. Our results support the hypothesis that depression and suicidality, apparent human universals, are credible signals of need that elicit more support than verbal requests, sad expressions, and crying when there are conflicts of interest.     

Honest signalling through chemicals by elephants with applications for care and conservation

Chemical signals are difficult to fake because they are often directly associated with phenotype and physiological condition, and hence likely to be honest signals for intraspecific communication. Chemical signals may be modified after release by the sender or by the environment. The proximate and ultimate signal meanings are dependent not only on the condition of the sender, but also on the physiological status of the receiver. Understanding the relationships and linkage among signal modality, signal function and receiver response is an essential first step before using natural signals for animal care and conservation. Our studies on chemical communication in Asian and African elephants combine observational and experimental work in captive and wild settings to further this understanding. Recent discoveries of pheromones in Asian elephants and the biochemistry of these compounds provide strong evidence that such chemical signals are honest indicators of reproductive status. Chemically identifying the signals and verifying their functional context with statistically robust behavioural studies are essential aspects for understanding the communication system. Additionally, the investigative process of discovering, identifying and verifying the function of chemical signals among captive elephants offers safe and stimulating enrichments. The knowledge garnered from such studies has potential conservation benefits for managing wild elephant populations. A firm foundation of scientific information is required for successful behavioural investigations and applied conservation and enrichment components.     

Costs and constraints conspire to produce honest signaling: insights from an ant queen pheromone

Signal costs and evolutionary constraints have both been proposed as ultimate explanations for the ubiquity of honest signaling, but the interface between these two factors is unclear. Here, I propose a pluralistic interpretation, and use game theory to demonstrate that evolutionary constraints determine whether signals evolve to be costly or cheap. Specifically, when the costs or benefits of signaling are strongly influenced by the sender's quality, low-cost signals evolve. The model reaffirms that cheap and costly signals can both be honest, and predicts that expensive signals should have more positive allometric slopes than cheap ones. The new framework is applied to an experimental study of an ant queen pheromone that honestly signals fecundity. Juvenile hormone was found to have opposing, dose-dependent effects on pheromone production and fecundity and was fatal at high doses, indicating that endocrine-mediated trade-offs preclude dishonesty. Several lines of evidence suggest that the realized cost of pheromone production may be nontrivial, and the antagonistic effects of juvenile hormone indicate the presence of significant evolutionary constraints. I conclude that the honesty of queen pheromones and other signals is likely enforced by both the cost of dishonesty and a suite of evolutionary constraints.     

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.     

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.     

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.     

Population variation and genetic control of pheromone communication systems in moths

The nature of variation in moth pheromone communication systems and its genetic control is critical for the evolution of these systems and for their role in mate-finding and reproductive isolation. Significant additive genetic variance has been demonstrated in female pheromone production in monomorphic populations. However, corresponding variance in male pheromone response with respect to the blend which is most active, appears to be low, as can be expected from the general asymmetry of sexual selection. Pheromone polymorphism and differences in communication systems between closely related species seem to be controlled by a small number of Mendelian genes. The critical biosynthetic steps, which are influenced by the genes controlling pheromone production, can be inferred from our present knowledge of pheromone biosynthesis. A mechanistic understanding of how male response to pheromones is controlled is further away. Failure to demonstrate genes with pleiotropic effects on critical sender and receiver traits, suggests that reciprocal selection on genetically independent sender and receiver loci is the more likely explanation for the generally observed coordination between pheromone production and response in moth populations. Further research on the evolutionary significance of Z-linked pheromone response genes, documented in several species, should be encouraged. Investigations, in the field, of populations that vary in pheromone production and response, and theoretical and empirical studies of the survival of sender and receiver mutants in otherwise monomorphic populations are also important to advance our understanding of how pheromone communication systems evolve.     

Phylogenetic analysis of the evolution of a signal of aggressive intent in northern swordtail fishes

The initiation of a coevolutionary relationship between signal and response can be explained by either the receiver taking advantage of information inadvertently provided by the sender or the sender taking advantage of a perceptual bias in the receiver. In addition, once both signal and response are present, the exchange of information may or may not be cooperative. We examined the evolution of a signal of aggressive intent (expression of vertical bars) across all the northern swordtail fishes (Xiphophorus) in a phylogenetic context. We found that the signal was present before responses evolved, which suggests that this coevolutionary relationship was initiated by the receiver taking advantage of information inadvertently provided by the signaler. In addition, we introduce a novel method for examining the cooperative nature of signaling systems and provide some evidence to suggest that in this signaling system, receivers may be exploiting an honest signal in some species.     

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.     

Beyond illness: Variation in haemosporidian load explains differences in vocal performance in a songbird

In animal communication, signals are expected to evolve to be honest, so that receivers avoid being manipulated by signalers. One way that signals can evolve to be honest is for them to be costly, with only high‐quality individuals being able to bear the costs of signal expression. It has been proposed that parasites can introduce costs that affect the expression of sexually selected traits, and there is evidence to support the role of parasitism in modulating animal behavior. If host infection status or intensity is found to relate to differences in signal expression, it may indicate a fitness cost that mediates honesty of signals. Birdsong is a good model for testing this, and physically challenging songs representing complex motor patterns provide a good example of sexually selected traits indicating individual condition. We performed a field study to evaluate the relationship between song performance and avian malaria infection in a common songbird. Previous work on this subject has almost always evaluated avian malaria in terms of binary infection status; however, parasitemia—infection intensity—is rarely assessed, even though differences in parasite load may have profound physiological consequences. We estimated parasitemia levels by using real‐time PCR. We found that birds with higher parasitemia displayed lower vocal performance, providing evidence that this song trait is an honest signal of parasitic load of haemosporidian parasites. To our knowledge, this study links parasite load and the expression of a sexually selected trait in a way that has not been addressed in the past. Studies using song performance traits and parasitemia offer an important perspective for understanding evolution of characters via sexual selection.     

The Handicap Principle: how an erroneous hypothesis became a scientific principle

The most widely cited explanation for the evolution of reliable signals is Zahavi's so‐called Handicap Principle, which proposes that signals are honest because they are costly to produce. Here we provide a critical review of the Handicap Principle and its theoretical development. We explain why this idea is erroneous, and how it nevertheless became widely accepted as the leading explanation for honest signalling. In 1975, Zahavi proposed that elaborate secondary sexual characters impose ‘handicaps’ on male survival, not due to inadvertent signalling trade‐offs, but as a mechanism that functions to demonstrate males' genetic quality to potential mates. His handicap hypothesis received many criticisms, and in response, Zahavi clarified his hypothesis and explained that it assumes that signals are wasteful as well as costly, and that they evolve because wastefulness enforces honesty. He proposed that signals evolve under ‘signal selection’, a non‐Darwinian type of selection that favours waste rather than efficiency. He maintained that the handicap hypothesis provides a general principle to explain the evolution of all types of signalling systems, i.e. the Handicap Principle. In 1977, Zahavi proposed a second hypothesis for honest signalling, which received many different labels and interpretations, although it was assumed to be another example of handicap signalling. In 1990, Grafen published models that he claimed vindicated Zahavi's Handicap Principle. His conclusions were widely accepted and the Handicap Principle subsequently became the dominant paradigm for explaining the evolution of honest signalling in the biological and social sciences. Researchers have subsequently focused on testing predications of the Handicap Principle, such as measuring the absolute costs of honest signals (and using energetic and other proximate costs as proxies for fitness), but very few have attempted to test Grafen's models. We show that Grafen's models do not support the handicap hypothesis, although they do support Zahavi's second hypothesis, which proposes that males adjust their investment into the expression of their sexual signals according to their condition and ability to bear the costs (and risks to their survival). Rather than being wasteful over‐investments, honest signals evolve in this scenario because selection favours efficient and optimal investment into signal expression and minimizes signalling costs. This idea is very different from the handicap hypothesis, but it has been widely misinterpreted and equated to the Handicap Principle. Theoretical studies have since shown that signalling costs paid at the equilibrium are neither sufficient nor necessary to maintain signal honesty, and that honesty can evolve through differential benefits, as well as differential costs. There have been increasing criticisms of the Handicap Principle, but they have focused on the limitations of Grafen's model and overlooked the fact that it is not a handicap model. This model is better understood within a Darwinian framework of adaptive signalling trade‐offs, without the added burden and confusing logic of the Handicap Principle. There is no theoretical or empirical support for the Handicap Principle and the time is long overdue to usher this idea into an ‘honorable retirement’.     

The signaller's dilemma: a cost-benefit analysis of public and private communication

Background

Understanding the diversity of animal signals requires knowledge of factors which may influence the different stages of communication, from the production of a signal by the sender up to the detection, identification and final decision-making in the receiver. Yet, many studies on signalling systems focus exclusively on the sender, and often ignore the receiver side and the ecological conditions under which signals evolve.

Methodology/Principal Findings

We study a neotropical katydid which uses airborne sound for long distance communication, but also an alternative form of private signalling through substrate vibration. We quantified the strength of predation by bats which eavesdrop on the airborne sound signal, by analysing insect remains at roosts of a bat family. Males do not arbitrarily use one or the other channel for communication, but spend more time with private signalling under full moon conditions, when the nocturnal rainforest favours predation by visually hunting predators. Measurements of metabolic CO₂-production rate indicate that the energy necessary for signalling increases 3-fold in full moon nights when private signalling is favoured. The background noise level for the airborne sound channel can amount to 70 dB SPL, whereas it is low in the vibration channel in the low frequency range of the vibration signal. The active space of the airborne sound signal varies between 22 and 35 meters, contrasting with about 4 meters with the vibration signal transmitted on the insect''s favourite roost plant. Signal perception was studied using neurophysiological methods under outdoor conditions, which is more reliable for the private mode of communication.

Conclusions/Significance

Our results demonstrate the complex effects of ecological conditions, such as predation, nocturnal ambient light levels, and masking noise levels on the performance of receivers in detecting mating signals, and that the net advantage or disadvantage of a mode of communication strongly depends on these conditions.     

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.     

Evolution of honest reward signal in flowers

Some flowering plants signal the abundance of their rewards by changing their flower colour, scent or other floral traits as rewards are depleted. These floral trait changes can be regarded as honest signals of reward states for pollinators. Previous studies have hypothesized that these signals are used to maintain plant-level attractiveness to pollinators, but the evolutionary conditions leading to the development of honest signals have not been well investigated from a theoretical basis. We examined conditions leading to the evolution of honest reward signals in flowers by applying a theoretical model that included pollinator response and signal accuracy. We assumed that pollinators learn floral traits and plant locations in association with reward states and use this information to decide which flowers to visit. While manipulating the level of associative learning, we investigated optimal flower longevity, the proportion of reward and rewardless flowers, and honest- and dishonest-signalling strategies. We found that honest signals are evolutionarily stable only when flowers are visited by pollinators with both high and low learning abilities. These findings imply that behavioural variation in learning within a pollinator community can lead to the evolution of an honest signal even when there is no contribution of rewardless flowers to pollinator attractiveness.     

Warning signals evolve to disengage Batesian mimics

Prey that are unprofitable to attack are typically conspicuous in appearance. Conventional theory assumes that these warning signals have evolved in response to predator receiver biases. However, such biases might be a symptom rather than a cause of warning signals. We therefore examine an alternative theory: that conspicuousness evolves in unprofitable prey to avoid confusion with profitable prey. One might wonder why unprofitable prey do not find a cryptic means to be distinct from profitable prey, reducing both their risk of confusion with profitable prey and their rate of detection by predators. Here we present the first coevolutionary model to allow for Batesian mimicry and signals with different levels of detectability. We find that unprofitable prey do indeed evolve ways of distinguishing themselves using cryptic signals, particularly when appearance traits can evolve in multiple dimensions. However, conspicuous warning signals readily evolve in unprofitable prey when there are more ways to look different from the background than to match it. Moreover, the more unprofitable the prey species, the higher its evolved conspicuousness. Our results provide strong support for the argument that unprofitable species evolve conspicuous signals to avoid confusion with profitable prey and indicate that peak shift in conspicuousness-linked traits is a major factor in its establishment.     

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.     

Coevolution of functionally constrained characters: prerequisites for adaptive versatility

One of the major problems of organismic evolution theory is to explain how complex organisms were able to evolve by random mutations in spite of the severe functional constraints that canalize their route of change. The problem is discussed on the basis of a quantitative genetic model. How the degree of genetic variation influences the adaptation speed of functionally coupled but genetically uncorrelated characters is examined. It was found, that if more than three independent characters contribute to the variation of a functionally constrained system, optimal degrees of genetic variation exist. Higher degrees of variation lead to decreasing adaptation rates. Conversely, functional constraints do not limit the degree of adaptely reasonable genetic variability as long as the number of independent characters is not higher than three. The conclusion is drawn that there is no need to develop a genetic correlation between functionally coupled characters as long as not many more than three characters are integrated into a functional system. This explains the fact that there is no genetic coupling between the inherited signal sender and receiver mechanisms in orthopterians, even though there is a strong functional coupling between them.     

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.     

Common language or Tower of Babel? On the evolutionary dynamics of signals and their meanings.

We investigate how the evolution of communication strategies affects signal credibility when there is common interest as well as a conflict between communicating individuals. Taking alarm calls as an example, we show that if the temptation to cheat is low, a single signal is used in the population. If the temptation increases cheaters will erode the credibility of a signal, and an honest mutant using a different signal ('a private code') will be very successful until this, in turn, is cracked by cheaters. In such a system, signal use fluctuates in time and space and hence the meaning of a given signal is not constant. When the temptation to cheat is too large, no honest communication can maintain itself in a Tower of Babel of many signals. We discuss our analysis in the light of the Green Beard mechanism for the evolution of altruism.