Honesty in signalling games is maintained by trade-offs rather than costs.

BACKGROUND: Signal reliability poses a central problem for explaining the evolution of communication. According to Zahavi's Handicap Principle, signals are honest only if they are costly at the evolutionary equilibrium; otherwise, deception becomes common and communication breaks down. Theoretical signalling games have proved to be useful for understanding the logic of signalling interactions. Theoretical evaluations of the Handicap Principle are difficult, however, because finding the equilibrium cost function in such signalling games is notoriously complicated. Here, we provide a general solution to this problem and show how cost functions can be calculated for any arbitrary, pairwise asymmetric signalling game at the evolutionary equilibrium. RESULTS: Our model clarifies the relationship between signalling costs at equilibrium and the conditions for reliable signalling. It shows that these two terms are independent in both additive and multiplicative models, and that the cost of signalling at honest equilibrium has no effect on the stability of communication. Moreover, it demonstrates that honest signals at the equilibrium can have any cost value, even negative, being beneficial for the signaller independently of the receiver's response at equilibrium and without requiring further constraints. Our results are general and we show how they apply to seminal signalling models, including Grafen's model of sexual selection and Godfray's model of parent-offspring communication. CONCLUSIONS: Our results refute the claim that signals must be costly at the evolutionary equilibrium to be reliable, as predicted by the Handicap Principle and so-called 'costly signalling' theory. Thus, our results raise serious concerns about the handicap paradigm. We argue that the evolution of reliable signalling is better understood within a Darwinian life-history framework, and that the conditions for honest signalling are more clearly stated and understood by evaluating their trade-offs rather than their costs per se. We discuss potential shortcomings of equilibrium models and we provide testable predictions to help advance the field and establish a better explanation for honest signals. Last but not least, our results highlight why signals are expected to be efficient rather than wasteful.

Condition-dependent trade-offs maintain honest signalling.

How and why animals and humans signal reliably is a key issue in biology and social sciences that needs to be understood to explain the evolution of communication. In situations in which the receiver needs to differentiate between low- and high-quality signallers, once a ruling paradigm, the Handicap Principle has claimed that honest signals have to be costly to produce. Subsequent game theoretical models, however, highlighted that honest signals are not necessarily costly. Honesty is maintained by the potential cost of cheating: by the difference in the marginal benefit to marginal cost for low versus high-quality signallers; i.e. by differential trade-offs. Owing to the difficulties of manipulating signal costs and benefits, there is lack of empirical tests of these predictions. We present the results of a laboratory decision-making experiment with human participants to test the role of equilibrium signal cost and signalling trade-offs for the development of honest communication. We found that the trade-off manipulation had a much higher influence on the reliability of communication than the manipulation of the equilibrium cost of signal. Contrary to the predictions of the Handicap Principle, negative production cost promoted honesty at a very high level in the differential trade-off condition.

Advertising cooperative phenotype through costly signals facilitates collective action.

Around the world, people engage in practices that involve self-inflicted pain and apparently wasted resources. Researchers theorized that these practices help stabilize within-group cooperation by assorting individuals committed to collective action. While this proposition was previously studied using existing religious practices, we provide a controlled framework for an experimental investigation of various predictions derived from this theory. We recruited 372 university students in the Czech Republic who were randomly assigned into either a high-cost or low-cost condition and then chose to play a public goods game (PGG) either in a group that wastes money to signal commitment to high contributions in the game or to play in the group without such signals. We predicted that cooperators would assort in the high-cost revealed group and that, despite these costs, they would contribute more to the common pool and earn larger individual rewards over five iterations of PGG compared with the concealed group and participants in the low-cost condition. The results showed that the assortment of cooperators was more effective in the high-cost condition and translated into larger contributions of the remaining endowment to the common pool, but participants in the low-cost revealed group earned the most. We conclude that costly signals can serve as an imperfect assorting mechanism, but the size of the costs needs to be carefully balanced with potential benefits to be profitable.

Cooperation as a signal of time preferences.

Many evolutionary models explain why we cooperate with non-kin, but few explain why cooperative behaviour and trust vary. Here, we introduce a model of cooperation as a signal of time preferences, which addresses this variability. At equilibrium in our model (i) future-oriented individuals are more motivated to cooperate, (ii) future-oriented populations have access to a wider range of cooperative opportunities, and (iii) spontaneous and inconspicuous cooperation reveal stronger preference for the future, and therefore inspire more trust. Our theory sheds light on the variability of cooperative behaviour and trust. Since affluence tends to align with time preferences, results (i) and (ii) explain why cooperation is often associated with affluence, in surveys and field studies. Time preferences also explain why we trust others based on proxies for impulsivity, and, following result (iii), why uncalculating, subtle and one-shot cooperators are deemed particularly trustworthy. Time preferences provide a powerful and parsimonious explanatory lens, through which we can better understand the variability of trust and cooperation.

Cooperating to show that you care: costly helping as an honest signal of fitness interdependence.

Social organisms often need to know how much to trust others to cooperate. Organisms can expect cooperation from another organism that depends on them (i.e. stake or fitness interdependence), but how do individuals assess fitness interdependence? Here, we extend fitness interdependence into a signalling context: costly helping behaviour can honestly signal one's stake in others, such that those who help are trusted more. We present a mathematical model in which agents help others based on their stake in the recipient's welfare, and recipients use that information to assess whom to trust. At equilibrium, helping is a costly signal of stake: helping is worthwhile for those who value the recipient (and thus will repay any trust), but is not worthwhile for those who do not value the recipient (and thus will betray the trust). Recipients demand signals when they value the signallers less and when the cost of betrayed trust is higher; signal costs are higher when signallers have more incentive to defect. Signalling systems are more likely when the trust games resemble Prisoner's Dilemmas, Stag Hunts or Harmony Games, and are less likely in Snowdrift Games. Furthermore, we find that honest signals need not benefit recipients and can even occur between hostile parties. By signalling their interdependence, organisms benefit from increased trust, even when no future interactions will occur. This article is part of the theme issue 'The language of cooperation: reputation and honest signalling'.

When does reputation lie? Dynamic feedbacks between costly signals, social capital and social prominence.

Performing a dramatic act of religious devotion, creating an art exhibit, or releasing a new product are all examples of public acts that signal quality and contribute to building a reputation. Signalling theory predicts that these public displays can reliably reveal quality. However, data from ethnographic work in South India suggests that more prominent individuals gain more from reputation-building religious acts than more marginalized individuals. To understand this phenomenon, we extend signalling theory to include variation in people's social prominence or social capital, first with an analytical model and then with an agent-based model. We consider two ways in which social prominence/capital may alter signalling: (i) it impacts observers' priors, and (ii) it alters the signallers' pay-offs. These two mechanisms can result in both a 'reputational shield,' where low quality individuals are able to 'pass' as high quality thanks to their greater social prominence/capital, and a 'reputational poverty trap,' where high quality individuals are unable to improve their standing owing to a lack of social prominence/capital. These findings bridge the signalling theory tradition prominent in behavioural ecology, anthropology and economics with the work on status hierarchies in sociology, and shed light on the complex ways in which individuals make inferences about others. This article is part of the theme issue 'The language of cooperation: reputation and honest signalling'.

A branded bandage is worth a thousand words: blood branded bandages signal men's generosity and morality.

BACKGROUND AND OBJECTIVE: Recruiting and retaining male donors remain an ongoing challenge for blood collection agencies. Research suggests that interventions based on costly signalling theory that allows donors to unobtrusively but publicly signal their donor status may be effective. However, what functions as such a signal and how it is interpreted has not been determined. MATERIALS AND METHODS: A total of 242 Australian residents (127 female; 115 male) recruited through an online research platform rated their perceptions of a male target wearing (a) no bandage, (b) a regular unmarked bandage or (c) a blood donor branded bandage. RESULTS: The target wearing a blood donor branded bandage was rated as significantly more generous by female participants and moral compared to both the target who wore no bandage and the target wearing a regular unmarked bandage. The target wearing the unmarked bandage was perceived as significantly less healthy and competent compared to the target not wearing a bandage. CONCLUSION: A public signal of public donor status conveys the generosity and morality of the wearer. The bandage applied to donors after they have donated can act as such an effective signal, but only when these bandages are clearly branded as resulting from donating blood.

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'.

Trophy hunters pay more to target larger-bodied carnivores.

Hunters often target species that require resource investment disproportionate to associated nutritional rewards. Costly signalling theory provides a potential explanation, proposing that hunters target species that impose high costs (e.g. higher failure and injury risks, lower consumptive returns) because it signals an ability to absorb costly behaviour. If costly signalling is relevant to contemporary 'big game' hunters, we would expect hunters to pay higher prices to hunt taxa with higher perceived costs. Accordingly, we hypothesized that hunt prices would be higher for taxa that are larger-bodied, rarer, carnivorous, or described as dangerous or difficult to hunt. In a dataset on 721 guided hunts for 15 North American large mammals, prices listed online increased with body size in carnivores (from approximately $550 to $1800 USD/day across the observed range). This pattern suggests that elements of costly signals may persist among contemporary non-subsistence hunters. Persistence might simply relate to deception, given that signal honesty and fitness benefits are unlikely in such different conditions compared with ancestral environments in which hunting behaviour evolved. If larger-bodied carnivores are generally more desirable to hunters, then conservation and management strategies should consider not only the ecology of the hunted but also the motivations of hunters.

A sheep in wolf's clothing: levels of deceit and detection in the evolution of cue-mimicry.

In an evolutionary context, trusted signals or cues provide individuals with the opportunity to manipulate them to their advantage by deceiving others. The deceived can then respond to the deception by either ignoring the signals or cues or evolving means of deception-detection. If the latter happens, it can result in an arms race between deception and detection. Here, we formally analyse these possibilities in the context of cue-mimicry in prey-predator interactions. We demonstrate that two extrinsic parameters control whether and for how long an arms race continues: the benefits of deception, and the cost of ignoring signals and cues and having an indiscriminate response. As long as the cost of new forms of deception is less than its benefits and the cost of new forms of detection is less than the cost of an indiscriminate response, an arms race results in the perpetual evolution of better forms of detection and deception. When novel forms of deception or detection become too costly to evolve, the population settles on a polymorphic equilibrium involving multiple strategies of deception and honesty, and multiple strategies of detection and trust.

A general model of biological signals, from cues to handicaps.

Organisms sometimes appear to use extravagant traits, or "handicaps", to signal their quality to an interested receiver. Before they were used as signals, many of these traits might have been selected to increase with individual quality for reasons apart from conveying information, allowing receivers to use the traits as "cues" of quality. However, current theory does not explain when and why cues of individual quality become exaggerated into costly handicaps. We address this here, using a game-theoretic model of adaptive signalling. Our model predicts that: (1) signals will honestly reflect signaler quality whenever there is a positive relationship between individual quality and the signalling trait's naturally selected, non-informational optimum; and (2) the slope of this relationship will determine the amount of costly signal exaggeration, with more exaggeration favored when the slope is more shallow. A shallow slope means that a lower quality male would pay only a small fitness cost to have the same trait value as a higher quality male, and this drives the exaggeration of signals as high-quality signalers are selected to distinguish themselves. Our model reveals a simple and potentially widespread mechanism for ensuring signal honesty and predicts a natural continuum of signalling strategies, from cost-free cues to costly handicaps.

State-dependent risk-taking.

Who takes risks, and when? The relative state model proposes two non-independent selection pressures governing risk-taking: need-based and ability-based. The need-based account suggests that actors take risks when they cannot reach target states with low-risk options (consistent with risk-sensitivity theory). The ability-based account suggests that actors engage in risk-taking when they possess traits or abilities that increase the expected value of risk-taking (by increasing the probability of success, enhancing payoffs for success or buffering against failure). Adaptive risk-taking involves integrating both considerations. Risk-takers compute the expected value of risk-taking based on their state-the interaction of embodied capital relative to one's situation, to the same individual in other circumstances or to other individuals. We provide mathematical support for this dual pathway model, and show that it can predict who will take the most risks and when (e.g. when risk-taking will be performed by those in good, poor, intermediate or extreme state only). Results confirm and elaborate on the initial verbal model of state-dependent risk-taking: selection favours agents who calibrate risk-taking based on implicit computations of condition and/or competitive (dis)advantage, which in turn drives patterned individual differences in risk-taking behaviour.

Altruism predicts mating success in humans.

In order for non-kin altruism to evolve, altruists must receive fitness benefits for their actions that outweigh the costs. Several researchers have suggested that altruism is a costly signal of desirable qualities, such that it could have evolved by sexual selection. In two studies, we show that altruism is broadly linked with mating success. In Study 1, participants who scored higher on a self-report altruism measure reported they were more desirable to the opposite sex, as well as reported having more sex partners, more casual sex partners, and having sex more often within relationships. Sex moderated some of these relationships, such that altruism mattered more for men's number of lifetime and casual sex partners. In Study 2, participants who were willing to donate potential monetary winnings (in a modified dictator dilemma) reported having more lifetime sex partners, more casual sex partners, and more sex partners over the past year. Men who were willing to donate also reported having more lifetime dating partners. Furthermore, these patterns persisted, even when controlling for narcissism, Big Five personality traits, and socially desirable responding. These results suggest that altruists have higher mating success than non-altruists and support the hypothesis that altruism is a sexually selected costly signal of difficult-to-observe qualities.

Are aposematic signals honest? A review.

We explore the relevance of honest signalling theory to the evolution of aposematism. We begin with a general consideration of models of signal stability, with a focus on the Zahavian costly signalling framework. Next, we review early models of signalling in the context of aposematism (some that are consistent and some inconsistent with costly honest signalling). We focus on controversies surrounding the idea that aposematic signals are handicaps in a Zahavian framework. Then, we discuss how the alignment of interests between signaller and predator influences the evolution of aposematism, highlight the distinction between qualitative and quantitative honesty and review theory and research relevant to these categories. We also review recent theoretical treatments of the evolution of aposematism that have focused on honest signalling as well as empirical research on a variety of organisms, including invertebrates and frogs. Finally, we discuss future directions for empirical and theoretical research in this area.

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.

Successful hunting increases testosterone and cortisol in a subsistence population.

Controversy over the adaptive significance of male hunting in subsistence societies hinges on the relative importance of familial provisioning and mate-quality signalling. This paper examines the proximate and ultimate motivations of hunting behaviour from a neuroendocrine perspective, using salivary testosterone and cortisol data collected before, during and after hunting focal follows from 31 Tsimane hunters aged 18-82 years. Despite circadian declines in hormone levels, testosterone and cortisol of Tsimane hunters increased at the time of a kill, and remained high as successful hunters returned home. Previous studies of hormonal changes during competitions find that high-stakes and success in the presence of relevant audiences result in increased neuroendocrine arousal. If men hunt primarily to provision their families, then an additional audience would not be expected to impact testosterone or cortisol, nor would the size of the animal killed. However, if signalling male quality by 'showing off' was a larger relative driver of men's hunting behaviour, one would expect greater hormonal response in cases where men returned with large sharable kills, especially in the presence of community members. Consistent with provisioning models of male hunting motivation, neither kill size nor encountering an audience of villagers while returning from hunting was associated with hormonal changes for successful hunters.

Honest signalling with costly gambles.

Costly signalling theory is commonly invoked as an explanation for how honest communication can be stable when interests conflict. However, the signal costs predicted by costly signalling models often turn out to be unrealistically high. These models generally assume that signal cost is determinate. Here, we consider the case where signal cost is instead stochastic. We examine both discrete and continuous signalling games and show that, under reasonable assumptions, stochasticity in signal costs can decrease the average cost at equilibrium for all individuals. This effect of stochasticity for decreasing signal costs is a fundamental mechanism that probably acts in a wide variety of circumstances.