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.     

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.     

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.     

Attention-Seeking Displays

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

Content,cost, and context: A framework for understanding human signaling systems

Humans frequently perform extravagant and seemingly costly behaviors, such as widely sharing hunted resources, erecting conspicuous monumental structures, and performing dramatic acts of religious devotion. Evolutionary anthropologists and archeologists have used signaling theory to explain the function of such displays, drawing inspiration from behavioral ecology, economics, and the social sciences. While signaling theory is broadly aimed at explaining honest communication, it has come to be strongly associated with the handicap principle, which proposes that such costly extravagance is in fact an adaptation for signal reliability. Most empirical studies of signaling theory have focused on obviously costly acts, and consequently anthropologists have likely overlooked a wide range of signals that also promote reliable communication. Here, we build on recent developments in signaling theory and animal communication, developing an updated framework that highlights the diversity of signal contents, costs, contexts, and reliability mechanisms present within human signaling systems. By broadening the perspective of signaling theory in human systems, we strive to identify promising areas for further empirical and theoretical work.     

How costly is the honest signaling of need?

ESS models of biological signaling have shown that costly signals can provide honest information. In the context of parent-offspring conflict over the allocation of resources by parents to their young, the theory explains costly offspring solicitation behavior as an accurate signal of offspring need to parents who cannot assess offspring condition directly. In this paper, we provide a simple but general characterization of the honest signaling of need in models of parent-offspring conflict: the offspring's signaling cost is proportional to the parent's fitness loss from satisfying the offspring's resource requirement. The factor of proportionality is given by a measure of the extent of parent-offspring conflict that depends only on coefficients of relatedness. These results hold for interbrood conflict with uniparental investment even if the relationship between offspring condition and resource requirement is not monotonic, and extend to cases of biparental care, uncertainty concerning the parent's condition, and intra-brood conflict. Copyright 1999 Academic Press.     

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.     

Costly signalling theories: beyond the handicap principle

Two recent overviews of costly signalling theory—Maynard-Smith and Harper (2003) and Searcy and Nowicki (2005)—both refuse to count signals kept honest by punishment of dishonesty, as costly signals, because (1) honest signals must be costly in cases of costly signalling, and (2) punishment of dishonesty itself requires explanation. I argue that both pairs of researchers are mistaken: (2) is not a reason to discount signals kept honest by punishment of dishonesty as cases of costly signalling, and (1) betrays too narrow a focus on certain versions of costly signalling theory. In the course of so arguing, I propose a new schema for classifying signal costs, which suggests productive research questions for future conceptual and empirical work on costly signalling.     

Costly signaling and torch fishing on Ifaluk atoll

In this paper I evaluate the merit of costly signaling theory (CST) as a paradigm for understanding why men of Ifaluk atoll torch fish. I argue that torch fishing is a handicap that signals men's productivity. Consistent with CST, torch fishing is observed by the predicted audience (women), energetically costly to perform, and a reliable indicator of the frequency a man fishes during the trade wind season. Contrary to expectations of who should benefit from torch fishing and consequently participate, torch fishers are not primarily young and unmarried. Torch fishers, however, are predominately from the matriline that owns the canoe on which they fish, suggesting that torch fishing also signals the productivity of a matriline. Although these results support the possibility that torch fishing is a handicap, no data are presented which demonstrate that torch fishers achieve any gains from sending the costly signal. This shortcoming and other directions for future research on Ifaluk foraging decisions are discussed.     

Influence of lighting environment on social preferences in sticklebacks from two different photic habitats.I.mate preferences of wild-caught females

Ultraviolet (UV) A signals (320–400 nm) are important in mate choice in numerous species. The sensitivity for UV signals is not only assumed to be costly, but also expected to be a function of the prevailing ecological conditions. Generally, those signals are favored by selection that efficiently reach the receiver. A decisive factor for color signaling is the lighting environment, especially in aquatic habitats, as the visibility of signals, and thus costs and benefits, are instantaneously influenced by it. Although ecological aspects of color signal evolution are relatively well-studied, there is little data on specific effects of environmental UV-light conditions on signaling at these shorter wavelengths. We studied wild-caught gravid female 3-spined sticklebacks Gasterosteus aculeatus of 2 photic habitat types (tea-stained and clear-water lakes), possessing great variation in their UV transmission. In 2 treatments, tea-stained and clear-water, preferences for males viewed under UV-present (UV+) and UV-absent (UV–) conditions were tested. A preference for males under UV+ conditions was found for females from both habitat types, thus stressing the significance of UV signals in stickleback’s mate choice decisions. However, females from both habitat types showed the most pronounced preferences for males under UV+ conditions under clear-water test conditions. Moreover, reflectance measurements revealed that the carotenoid-based orange-red breeding coloration in wild-caught males of both habitat types differed significantly in color intensity (higher in clear-water males) and hue (more red shifted in clear-water males) while no significant differences in UV coloration were found. The differential reflection patterns in longer wavelengths suggest that sticklebacks of both habitat types have adapted to the respective water conditions. Adaptations of UV signals in a sexual context to ambient light conditions in both behavior and coloration seem less evident.     

Contract theory for the evolution of cooperation: The right incentives attract the right partners

Partner choice is a critical stage of many biological interactions, from mating to cooperation. When the quality of the potential partners is unknown, one way to choose is to rely on signaling: costly signals can reveal the quality of the sender and allow the receiver to choose. In some cases, however, signaling (or an active choice based on signals) is not possible, for example in the initiation of the symbiosis between the squid Euprymna scolopes and the bioluminescent bacterium Vibrio fischeri. How is partner choice possible in this and other similar cases? I show that in a game with asymmetric information without signaling, imposing a deliberate cost for establishing the interaction allows the non-informed individual to attract the right partner if the cost induces only high quality individuals to accept the interaction. Furthermore, imposing different costs and rewards may induce the informed individuals to screen themselves according to their types, and therefore allow the non-informed individual to establish an association with the correct partners in the absence of signaling.     

THE COST OF SEXUAL SIGNALING IN YEAST

The handicap principle holds that costly sexual signals can reliably indicate mate quality. Only individuals of high quality can afford a strong signal—the cost of signaling is relatively lower for high‐quality signalers than for low‐quality signalers. This critical property is difficult to test experimentally because the benefit of signaling on mating success, and cost of signaling on other components of fitness, cannot easily be separated in obligate sexual organisms. We therefore studied the facultatively sexual yeast Saccharomyces cerevisiae, which produces pheromones to attract potential mates. To precisely measure the cost of signaling, the signal was reduced or removed by deleting one or both copies of the pheromone‐encoding genes and measuring asexual growth rate in competition with a wild‐type signaler. We manipulated signaler quality either by changing the quality of the assay environment or by changing the number of deleterious mutations carried. For both types of treatment, we found that the cost of signaling decreased as the quality of the signaler increased, demonstrating that the yeast pheromone signal has the key property required for selection under the handicap principle. We found that cells of high genetic quality produce stronger signals than low‐quality cells, verifying that the signal is indeed honest.     

Sexual conflict and the evolution of female preferences for indicators of male quality

Males and females have opposing interests when it comes to the honesty of signals used in mate choice. The existence of this sexual conflict has long been acknowledged, but its consequences have not been fully investigated. By applying adaptive dynamics methods and individual-based computer simulations to a standard model for good-genes sexual selection, we show that sexual conflict over condition-dependent signaling can prevent the handicap process from ever attaining an evolutionary equilibrium. We outline the parameter conditions and properties of the underlying genetics conducive to nonequilibrium behavior and discuss the potential of such behavior to explain the elaboration and frequent phylogenetic loss of sexually selected traits. We also evaluate its consequences for well-established insights of sexual selection theory previously shown to apply when female mating preference and male ornament expression do converge on stable equilibrium levels. Contrary to equilibrium expectation, a continual change of condition-dependent signaling enables the evolution of a costly preference for a pure epistatic indicator and the evolution of preferences for redundant signals or a large number of independent ornaments. We thus conclude that seemingly general results of sexual selection theory, insofar as these are based on equilibrium considerations, do not extend to cases where nonequilibrium behavior occurs.     

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.     

Errors drive the evolution of biological signalling to costly codes

Reduction of costs in biological signalling seems an evolutionary advantage, but recent experiments have shown signalling codes shifted to signals of high cost with an underutilization of low-cost signals. Here I derive a theory for efficient signalling that includes both errors and costs as constraints and I show that errors in the efficient translation of biological states into signals can shift codes to higher costs, effectively performing a quality control. The statistical structure of signal usage is predicted to be of a generalized Boltzmann form that penalizes signals that are costly and sensitive to errors. This predicted distribution of signal usage against signal cost has two main features: an exponential tail required for cost efficiency and an underutilization of the low-cost signals required to protect the signalling quality from the errors. These predictions are shown to correspond quantitatively to the experiments in which gathering signal statistics is feasible as in visual cortex neurons.     

Strong reciprocity, human cooperation, and the enforcement of social norms

This paper provides strong evidence challenging the self-interest assumption that dominates the behavioral sciences and much evolutionary thinking. The evidence indicates that many people have a tendency to voluntarily cooperate, if treated fairly, and to punish noncooperators. We call this behavioral propensity “strong reciprocity” and show empirically that it can lead to almost universal cooperation in circumstances in which purely self-interested behavior would cause a complete breakdown of cooperation. In addition, we show that people are willing to punish those who behaved unfairly towards a third person or who defected in a Prisoner’s Dilemma game with a third person. This suggests that strong reciprocity is a powerful device for the enforcement of social norms involving, for example, food sharing or collective action. Strong reciprocity cannot be rationalized as an adaptive trait by the leading evolutionary theories of human cooperation (in other words, kin selection, reciprocal altruism, indirect reciprocity, and costly signaling theory). However, multilevel selection theories of cultural evolution are consistent with strong reciprocity.     

Evolution of talking plants in a tritrophic context: conditions for uninfested plants to attract predators prior to herbivore attack

Herbivory induces plants to emit volatile chemicals that attract enemies of the herbivores (bodyguards of plants). In this way, the plant acquires protection and the bodyguards gain food. These plant signals cause neighboring plants, not under attack, to release signals as well. We hypothesize that such "secondary" signals help to reduce damage from future herbivore attacks by the protection received from the bodyguards. By modeling we explore the conditions for such secondary signals to evolve. Three kinds of strategies are considered: plants of the first strategy always emit a signal, those of the second strategy emit a signal only when infested, and those of the third strategy emit a signal not only when infested, but also when a certain number of neighbors are infested (i.e. secondary signaling). When signaling is much less (much more) costly than damage from herbivory, the first (second) strategy will be favored by selection, whereas for intermediate costs the third strategy, i.e. secondary signaling, will evolve. However, secondary signaling will not evolve when the primary signals lure the bodyguards too effectively. This is because the undamaged plant gains associational defense when the infested individual is defending very well; therefore, the need for secondary signaling decreases.     

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.     

Cheap talk when interests conflict

Most evolutionary analyses of animal communication suggest that low-cost signals can evolve only when both the signaller and the recipient rank outcomes in the same order. When there is a conflict of interest between sender and receiver, honest signals must be costly. However, recent work suggests that low-cost signals can be evolutionarily stable, even when the sender and the receiver rank outcomes in different orders, as long as the interest in achieving coordination is sufficiently great. In this paper, we extend this body of work by analysing a game theory model that shows that low-cost signals can evolve when there are conflicts of interest and no interest in coordination, as long as individuals interact repeatedly. We also present an empirical example indicating that female rhesus macaques, Macaca mulatta, use honest, low-cost, vocal signals to facilitate interactions when conflicts of interest exist. Copyright 2000 The Association for the Study of Animal Behaviour.     

Fame,fortune, and fitness at the Academy Awards

People across many societies routinely participate in physical or intellectual competitions in the absence of immediate substantial monetary or other apparent material rewards. But increased fame and social status associated with awards, such as the “Oscars”, need not be necessarily and solely a cultural construct unrelated to natural selection. Rather, prizes might be badges of honor if they are also honest indicators of evolutionary fitness. Analyses of reported reproductive success data, from a survey of well-known female and male actors, followed previously reported patterns of biological fitness in this sample of a human population. In addition, the numbers of Academy Awards received for acting were positively associated with reported numbers of biological children for both genders. The association of increased fitness with more awards received was statistically consistent even when considering that this subset of the population conformed to the Bateman effect in human reproduction: male actors had a more positive correlation than females between cumulative numbers of married partners and overall numbers of children. Honest signals of reproductive quality that are displayed by both sexes are expected to occur in humans and other species with costly biparental care and mutual mate choice.