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.     

Costly signaling and the handicap principle in hunter‐gatherer research: A critical review

It has been argued that men's hunting in many forager groups is not, primarily, a means of family provisioning but is a costly way of signaling otherwise cryptic qualities related to hunting ability. Much literature concerning the signaling value of hunting draws links to Zahavi's handicap principle and the costly signaling literature in zoology. However, although nominally grounded in the same theoretical paradigm, these literatures have evolved separately. Here I review honest signaling theory in both hunter‐gatherer studies and zoology and highlight three issues with the costly signaling literature in hunter‐gather studies: (a) an overemphasis on the demonstration of realized costs, which are neither necessary nor sufficient to diagnose costly signaling; (b) a lack of clear predictions about what specific qualities hunting actually signals; and (c) an insufficient focus on the broadcast effectiveness of hunting and its value as a heuristics for signal recipients. Rather than signaling hunting prowess, hunting might instead facilitate reputation‐building.     

OPTIMAL INVESTMENT IN SOCIAL SIGNALS

This study is an attempt to determine how much individuals should invest in social communication, depending on the type of relationships they may form. Two simple models of social relationships are considered. In both models, individuals emit costly signals to advertise their “quality” as potential friends. Relationships are asymmetrical or symmetrical. In the asymmetrical condition (first model), we observe that low‐quality individuals are discouraged from signaling. In the symmetrical condition (second model), all individuals invest in communication. In both models, high‐quality individuals (elite) do not compete and signal uniformly. The level of this uniform signal and the size of the “elite” turn out to be controlled by the accuracy of signals. The two models may be relevant to several aspects of animal and human social communication.     

Begging the question: are offspring solicitation behaviours signals of need?

Throughout the animal kingdom, distinctive behaviour by offspring commonly precedes and accompanies their provisioning by parents. Here, we assess empirical support for the recent theory that begging advertises offspring need, that parents provision young in relation to begging intensity, and that the apparently costly nature of begging ensures the reliability of the signal. While there is some support for the predictions of honest signalling models, empirical work has also revealed a host of complexities (such as the use of multiple signals) that existing theoretical analyses have only begun to address.     

Charitable giving as a signal of trustworthiness: Disentangling the signaling benefits of altruistic acts

It has been shown that psychological predispositions to benefit others can motivate human cooperation and the evolution of such social preferences can be explained with kin or multi-level selection models. It has also been shown that cooperation can evolve as a costly signal of an unobservable quality that makes a person more attractive with regard to other types of social interactions. Here we show that if a proportion of individuals with social preferences is maintained in the population through kin or multi-level selection, cooperative acts that are truly altruistic can be a costly signal of social preferences and make altruistic individuals more trustworthy interaction partners in social exchange. In a computerized laboratory experiment, we test whether altruistic behavior in the form of charitable giving is indeed correlated with trustworthiness and whether a charitable donation increases the observing agents' trust in the donor. Our results support these hypotheses and show that, apart from trust, responses to altruistic acts can have a rewarding or outcome-equalizing purpose. Our findings corroborate that the signaling benefits of altruistic acts that accrue in social exchange can ease the conditions for the evolution of social preferences.     

In the eye (and ears) of the beholder: Receiver psychology and human signal design

Although the study of signals has been part of human behavioral ecology since the field's inception,¹ only recently has signaling theory become important to the evolutionary study of human behavior and culture.² Signaling theory's rise to prominence has been propelled mainly by applications of costly signaling theory,³ which has shed light on a wide variety of human behaviors ranging from hunting⁴ to religion.^5,6 Costly signaling rests on the idea that wasteful but highly visible traits and behaviors can be explained as honest indicators of underlying qualities that are otherwise difficult to detect. For example, a laborious hunting technique may serve as a display of skill on the part of the hunter, who may then be favorably perceived by potential mates and allies.⁴ The costs of the activity ensure that the signal is honest, since unskilled hunters will not be able to perform as well. Despite the usefulness of this perspective, many such studies begin by documenting a costly behavior that is then explained with reference to costly signaling theory. Because such behaviors are easy to detect, they may be overemphasized in the literature.⁷ Moreover, costly signaling theory by itself can explain neither all signals nor all aspects of signal design. In this review, we argue that a focus on the role that the psychology of the intended receiver plays in signal design can expand the scope of signaling theory as a promising avenue to explain human behavior.     

Cost,expenditure and vulnerability

The handicap principle (HP) stipulates that signal reliability can be maintained if signals are costly to produce. Yet empirical biologists are typically unable to directly measure evolutionary costs, and instead appeal to expenditure (the time, energy and resources associated with signaling behavior) as a sensible proxy. However the link between expenditure and cost is not always as straightforward as proponents of HP assume. We consider signaling interactions where whether the expenditure associated with signaling is converted into an evolutionary cost is in some sense dependent on the behavior of the intended recipient of the signal. We illustrate this with a few empirical examples and demonstrate that on this alternative expenditure to cost mapping the traditional predictions of HP no longer hold. Instead of full information transfer, a partially informative communication system like those uncovered by Wagner (Games 4(2):163–181, 2013) and Zollman et al. (Proc R Soc B 20121878, 2012) is possible.     

Some mistakes go unpunished: the evolution of "all or nothing" signalling

Many models of honest signaling, based on Zahavi's handicap principle, predict that if receivers are interested in a quality that shows continuous variation across the population of signalers, then the distribution of signal intensities will also be continuous. However, it has previously been noted that this prediction does not agree with empirical observation in many signaling systems, where signals are limited to a small number of levels despite continuous variation in the trait being signaled. Typically, there is a critical value of the trait, with all individuals with trait values on one side of the threshold using the same cheap signal, and all those with trait values on the other side of the threshold using the same expensive signal. It has already been demonstrated that these classical models naturally predict such "all-or-nothing signaling" if it is additionally assumed that receivers suffer from perceptual error in evaluating signal strength. We show that such all-or-nothing signaling is also predicted if receivers are limited to responding to the signals in one of two ways. We suggest that many ecological situations (such as the decision to attack the signaler or not, or mate with the signaler or not) involve such binary choices.     

Costly apologies communicate conciliatory intention: an fMRI study on forgiveness in response to costly apologies

Reconciliation is an integral part of our social lives. Nevertheless, if a victim perceives the risk of further exploitation by his/her transgressor as non-negligible, the victim may well have difficulty forgiving the transgressor. Therefore, a key ingredient of reconciliation is the transgressor's sincere apology. Theoretical and empirical studies have shown that transgressors can make their apologies credible by incurring a substantial cost. Therefore, we hypothesized that costly apologies, compared to non-costly apologies (i.e., simply saying “sorry”), would effectively communicate a transgressor's conciliatory intention. In a functional magnetic resonance imaging (fMRI) study, participants were asked to imagine a friend committing a mild interpersonal transgression (e.g., standing up the participant) and then apologizing in a costly fashion, apologizing in a non-costly fashion, or not apologizing at all. Compared to non-costly apologies and non-apologies, costly apologies (signals of conciliatory intention) more strongly activated the theory-of-mind network (i.e., bilateral temporoparietal junction, precuneus, medial prefrontal cortex). Moreover, we did not observe any significant differences in brain responses to non-costly apologies and non-apology controls. These results underscore the importance of costly signals in human communication and in human peace-making in particular.     

Social benefits of luxury brands as costly signals of wealth and status

Drawing from costly signaling theory, we predicted that luxury consumption enhances status and produces benefits in social interactions. Across seven experiments, displays of luxury — manipulated through brand labels on clothes — elicited different kinds of preferential treatment, which even resulted in financial benefits to people who engaged in conspicuous consumption. Furthermore, we tested preconditions in which the beneficial consequences of conspicuous consumption may arise and determined the proximate mechanisms underlying them. The present data suggest that luxury consumption can be a profitable social strategy because conspicuous displays of luxury qualify as a costly signaling trait that elicits status-dependent favorable treatment in human social interactions.     

"Conventional" Signals in Avian Agonistic Displays: Integrating Theory, Data and Different Levels of Analysis

We present an integration of communication theory and data, drawing on examples from titmice (Aves: Paridae). We suggest how display actions such as lifting the head, raising the nape feathers, crest erecting and spreading the wings, act in agonistic communication when physical contact between opponents is rare. We propose that such displays largely act as strategic choice handicap signals. By giving these displays the signaller is believed to incur costs which underwrite the reliability of the signals; it may strategically increase these costs (for example by display repetition or adding additional elements) to signal its condition, motivation and hence the subjective value of a resource. It is shown that linking these ideas with earlier theories on the causation of display components, leads to an explanation of why birds have a greater repertoire of signals associated with aggression/winning, than with submission/losing. It is suggested that modellers of communication systems and those interested in the theory of signal design should pay more attention to the evolutionary constraints imposed by signal origin. Copyright 1999 Academic Press.     

Glutamate,Glutamate Receptors,and Downstream Signaling Pathways

Glutamate is a nonessential amino acid, a major bioenergetic substrate for proliferating normal and neoplastic cells, and an excitatory neurotransmitter that is actively involved in biosynthetic, bioenergetic, metabolic, and oncogenic signaling pathways. Glutamate signaling activates a family of receptors consisting of metabotropic glutamate receptors (mGluRs) and ionotropic glutamate receptors (iGluRs), both of which have been implicated in chronic disabling brain disorders such as Schizophrenia and neurodegenerative diseases like Alzheimer''s, Parkinson''s, and multiple sclerosis. In this review, we discuss the structural and functional relationship of mGluRs and iGluRs and their downstream signaling pathways. The three groups of mGluRs, the associated second messenger systems, and subsequent activation of PI3K/Akt, MAPK, NFkB, PLC, and Ca/CaM signaling systems will be discussed in detail. The current state of human mGluR1a as one of the most important isoforms of Group I-mGluRs will be highlighted. The lack of studies on the human orthologues of mGluRs family will be outlined. We conclude that upon further study, human glutamate-initiated signaling pathways may provide novel therapeutic opportunities for a variety of non-malignant and malignant human diseases.     

Honor and Violence

We present a theory of honor violence as a form of costly signaling. Two types of honor violence are identified: revenge and purification. Both types are amenable to a signaling analysis whereby the violent behavior is a signal that can be used by out-groups to draw inferences about the nature of the signaling group, thereby helping to solve perennial problems of social cooperation: deterrence and assurance. The analysis shows that apparently gratuitous acts of violence can be part of a system of norms that are Pareto superior to alternatives without such signals. For societies that lack mechanisms of governance to deter aggression or to enforce contracts, norms of honor can be a rational means of achieving these functions. The theory also suggests that cultures can become trapped in inefficient equilibria owing to path-dependent phenomena. In other words, costly signals of honor may continue to be sent even when they are no longer providing useful information.     

Microbial Communication,Cooperation and Cheating: Quorum Sensing Drives the Evolution of Cooperation in Bacteria

An increasing body of empirical evidence suggests that cooperation among clone-mates is common in bacteria. Bacterial cooperation may take the form of the excretion of “public goods”: exoproducts such as virulence factors, exoenzymes or components of the matrix in biofilms, to yield significant benefit for individuals joining in the common effort of producing them. Supposedly in order to spare unnecessary costs when the population is too sparse to supply the sufficient exoproduct level, many bacteria have evolved a simple chemical communication system called quorum sensing (QS), to “measure” the population density of clone-mates in their close neighborhood. Cooperation genes are expressed only above a threshold rate of QS signal molecule re-capture, i.e., above the local quorum of cooperators. The cooperative population is exposed to exploitation by cheaters, i.e., mutants who contribute less or nil to the effort but fully enjoy the benefits of cooperation. The communication system is also vulnerable to a different type of cheaters (“Liars”) who may produce the QS signal but not the exoproduct, thus ruining the reliability of the signal. Since there is no reason to assume that such cheaters cannot evolve and invade the populations of honestly signaling cooperators, the empirical fact of the existence of both bacterial cooperation and the associated QS communication system seems puzzling. Using a stochastic cellular automaton approach and allowing mutations in an initially non-cooperating, non-communicating strain we show that both cooperation and the associated communication system can evolve, spread and remain persistent. The QS genes help cooperative behavior to invade the population, and vice versa; cooperation and communication might have evolved synergistically in bacteria. Moreover, in good agreement with the empirical data recently available, this synergism opens up a remarkably rich repertoire of social interactions in which cheating and exploitation are commonplace.     

Natural gaze signaling in a social context

Evolutionary theory, augmented by a vast literature on gaze cuing and gaze following, suggests that the unique high-contrast morphology of the human eye evolved for rapid and silent communication between conspecifics. While this theory rests on the fundamental idea that humans use their eyes to signal information, empirical studies have focused exclusively on the effects of gaze cues on human receivers. In a series of three experiments we examined the other side of the communication dynamic by investigating if, and when, humans signal gaze information to other humans in a natural, but controlled, situation involving food consumption. First, we established that there is a normative behavior to look away when someone begins to bite. Second, we found that participants were significantly more likely to look down at their food before taking a bite when they were eating with another person versus alone. Lastly, we found that in pairs where a social connection has been established, when one person looks down signaling that a bite is forthcoming, the other person tends to look away. These results demonstrate that natural gaze signaling occurs in the context of eating, and it can, dependent on the relationship between the pair, trigger a gaze response that is different from gaze following. Our study shows that natural social attention between individuals is a two-way street, where each person can signal and read gaze information, consistent with the idea that human eye morphology evolved to facilitate communication between conspecifics.     

Relatedness influences signal reliability in evolving robots

Communication is an indispensable component of animal societies, yet many open questions remain regarding the factors affecting the evolution and reliability of signalling systems. A potentially important factor is the level of genetic relatedness between signallers and receivers. To quantitatively explore the role of relatedness in the evolution of reliable signals, we conducted artificial evolution over 500 generations in a system of foraging robots that can emit and perceive light signals. By devising a quantitative measure of signal reliability, and comparing independently evolving populations differing in within-group relatedness, we show a strong positive correlation between relatedness and reliability. Unrelated robots produced unreliable signals, whereas highly related robots produced signals that reliably indicated the location of the food source and thereby increased performance. Comparisons across populations also revealed that the frequency for signal production—which is often used as a proxy of signal reliability in empirical studies on animal communication—is a poor predictor of signal reliability and, accordingly, is not consistently correlated with group performance. This has important implications for our understanding of signal evolution and the empirical tools that are used to investigate communication.     

The establishment of communication systems depends on the scale of competition

How communication systems emerge and remain stable is an important question in both cognitive science and evolutionary biology. For communication to arise, not only must individuals cooperate by signaling reliable information, but they must also coordinate and perpetuate signals. Most studies on the emergence of communication in humans typically consider scenarios where individuals implicitly share the same interests. Likewise, most studies on human cooperation consider scenarios where shared conventions of signals and meanings cannot be developed de novo. Here, we combined both approaches with an economic experiment where participants could develop a common language, but under different conditions fostering or hindering cooperation. Participants endeavored to acquire a resource through a learning task in a computer-based environment. After this task, participants had the option to transmit a signal (a color) to a fellow group member, who would subsequently play the same learning task. We varied the way participants competed with each other (either global scale or local scale) and the cost of transmitting a signal (either costly or noncostly) and tracked the way in which signals were used as communication among players. Under global competition, players signaled more often and more consistently, scored higher individual payoffs, and established shared associations of signals and meanings. In addition, costly signals were also more likely to be used under global competition; whereas under local competition, fewer signals were sent and no effective communication system was developed. Our results demonstrate that communication involves both a coordination and a cooperative dilemma and show the importance of studying language evolution under different conditions influencing human cooperation.     

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.     

Ready to Fight: Reliable Predictors of Attack in a Cooperatively Breeding,Non‐Passerine Bird

Signal reliability is a major focus of animal communication research. Aggressive signals are ideal for measuring signal reliability because the signal referent – attack or no attack – can be measured unambiguously. Signals of aggressive intent occur at elevated rates in aggressive contexts, predict subsequent aggression by the signaler, and elicit appropriate responses from receivers. We tested the ‘predictive criterion’ in smooth‐billed anis, Crotophaga ani, by broadcasting one of two playback types (‘ahnee’ calls only or ‘ahnee + hoot’ calls), presenting a taxidermic mount, and observing the animals’ behavior. Based on the hypotheses that ‘hoot’ calls and ‘throat‐inflation’ displays signal aggressive intent, we predicted that they would be associated with attack, and that signaling rate would increase over the time period leading up to an attack. Indeed, both hoots and throat‐inflation displays reliably predicted attack. The second prediction, that signaling rate increases in the time leading up to attack, was strongly supported for throat‐inflation displays, which increased over the pre‐attack period in both treatments. Hoots increased over the pre‐attack period in ahnee playbacks but not in ahnee + hoot playbacks. Hierarchical signaling systems are characterized by early, less‐reliable predictors of attack, and later, more reliable predictors of attack. During both natural and simulated interactions, the more‐reliable throat‐inflation display tended to precede the less‐reliable hoot call, suggesting that this signaling system is not hierarchical. In a comparison of 11 putative signals of aggressive intent in birds, the throat‐inflation display had the second highest mutual information (reduction in uncertainty) among visual signals and non‐passerine signals while hoots had below‐average mutual information. Natural observations indicate that both hoots and throat‐inflation displays occur in the context of aggressive between‐group encounters, and hoots also occur during within‐group interactions. Throat‐inflation displays appear to be reliable indicators of aggressive intent, but the function of hoot calls is less clear.