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.     

Linking signal fidelity and the efficiency costs of communication

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

Scent-marking displays provide honest signals of health and infection

Males of many species produce scent marks and other olfactorysignals that function to intimidate rivals and attract females.It has been suggested that scent marks provide an honest, cheat-proofdisplay of an individual's health and condition. Here we reportseveral findings that address this hypothesis in wild-derivedhouse mice (Mus musculus domesticus). (1) We exposed males tofemale odor, which induces an increase in testosterone, andfound that sexual stimulation significantly increased the males'scent-marking and the attractiveness of their scent marks tofemales. (2) We challenged sexually stimulated males with anonreplicating strain of bacteria (Salmonella enterica C5TS)to activate immunity and found that this significantly decreasedthe males' scent-marking and the attractiveness of their scentmarks to females. (3) We collected scent marks from infectedand sham-infected males when they were sexually stimulated ornot, and we found that females could significantly discriminatethe scent marks of infected versus control males, but only whenthe males were sexually stimulated. Taken together, our resultsindicate that male mice modulate their scent-marking displaydepending on their health and perceived mating opportunities.Increased scent marking enhances males' attractiveness to females,scent marks provide an honest indicator of bacterial infection(and perhaps immune activation), and females are able to assessthe health of males more easily when males mark at a high rate.     

Investment in attending to cues and the evolution of amplifiers

Signals and cues are extensively used in social interactions across diverse communication systems. Here, we extend an existing theoretical framework to explore investment by emitters and perceivers in the fidelity with which cues and signals associated with the former are detected by the latter. Traits of the emitter that improve cue or signal fidelity without adding information are termed ‘amplifiers’. We assume that each party can invest in improving fidelity but that it is increasingly costly the more fidelity is improved. Our model predicts that evolution of amplifier traits of a pre‐existing cue occurs over a broader range of circumstances than evolution of signalling in situations where the emitter offered no pre‐existing cue to the perceiver. It further predicts that the greater the intrinsic informational value of a cue, the more likely it is that the perceiver (and not the emitter) will invest in the fidelity of detecting that cue. A consequence of this predicted asymmetry is that true communication with reciprocal adaptations in emitters and perceivers to improve signal fidelity is likely to occur predominantly for traits of intermediate reliability. The corollary is that uncertainty of the perceiver will then be a key feature of communication. Uncertainty can arise because perceivers misinterpret signals or do not perceive them correctly, but here we argue that uncertainty is more fundamentally at the root of communication because traits that are intrinsically highly informative will induce only the perceiver and not the emitter to invest in improved fidelity of perception of that trait.     

Sexual selection and the evolution of costly female preferences: spatial effects

Abstract.— Models of Fisher's runaway process show that if there is a cost to female preference, no preference or male trait exaggeration will evolve. Surprisingly, this is true no matter how small the cost, which reveals that these models of Fisher's process are structurally unstable (Bulmer 1989). Here a model of Fisher's runaway process is presented to demonstrate that costly female preference evolves very easily when space is explicitly included in the model. The only requirement is that the optimal male phenotype changes across the species' range. The model shows that the spatial average of the female preference and male trait reach an evolutionary equilibrium that is identical to those of nonspatial models, but that the preference and male trait can deviate greatly from these averages at any point in space. For example, if random mating results in the lowest cost to females, then at equilibrium the spatial average preference will be zero. Nevertheless, there will be some locations at which females prefer males with larger ornaments and others where they prefer males with smaller ornaments. Results also show that the structural instability of nonspatial models of Fisher's process is less of a problem in spatial models. In particular, many of the main qualitative features of cost-free spatial models of Fisher's process remain valid even when there are small costs of female preference. Finally, the model shows that abrupt changes in the optimal male phenotype across space can result in an amplification of this pattern when preference has a small cost, but it can also result in a pattern similar to reproductive character displacement. Which of these occurs depends on the magnitude of the cost of female preference. This suggests that some patterns of reproductive character displacement in nature might be explained simply by sexual selection rather than by hybrid dysgenesis and reinforcement.     

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’.     

Resolving current disagreements and ambiguities in the terminology of animal communication

Communication is central to most interactions between organisms. There is currently considerable controversy about the evolution, function and even about the most basic definition of communication. The controversy is linked to definitional ambiguities and disagreements. Here we discuss how some recent disagreements can be resolved and offer a clear set of definitions. Central to our approach is a definition of communication as being a trade between one organism (the informer) and another (the perceiver). The informer exerts influence on the perceiver through the communication process, and the perceiver experiences a change in its informational state (that is, gains information) as a consequence of detecting the communication. We define both influence and information explicitly and delineate between signalling, deceptive communication, and situations where perceivers respond to cues rather than signals. We demonstrate how our definitions allow resolution of conflicts arising in recent publications on the definitions on communication and related terms.     

Signaling,solidarity, and the sacred: The evolution of religious behavior

Anthropologists have repeatedly noted that there has been little theoretical progress in the anthropology of religion over the past fifty years.^1–7 By the 1960s, Geertz² had pronounced the field dead. Recently, however, evolutionary researchers have turned their attention toward understanding the selective pressures that have shaped the human capacity for religious thoughts and behaviors, and appear to be resurrecting this long‐dormant but important area of research.^8–19 This work, which focuses on ultimate evolutionary explanations, is being complemented by advances in neuropsychology and a growing interest among neuroscientists in how ritual, trance, meditation, and other altered states affect brain functioning and development.^20–26 This latter research is providing critical insights into the evolution of the proximate mechanisms responsible for religious behavior. Here we review these literatures and examine both the proximate mechanisms and ultimate evolutionary processes essential for developing a comprehensive evolutionary explanation of religion.     

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.     

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.     

On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality

In any given species, cooperation involves prosocial acts that usually return a fitness benefit to the actor. These acts are produced by a set of psychological rules, which will be similar in related species if they have a similar natural history of cooperation. Prosocial acts can be (i) reactive, i.e. in response to specific stimuli, or (ii) proactive, i.e. occur in the absence of such stimuli. We propose that reactive prosocial acts reflect sensitivity to (i) signals or signs of need and (ii) the presence and size of an audience, as modified by (iii) social distance to the partner or partners. We examine the evidence for these elements in humans and other animals, especially non-human primates, based on the natural history of cooperation, quantified in the context of food sharing, and various experimental paradigms. The comparison suggests that humans share with their closest living relatives reactive responses to signals of need, but differ in sensitivity to signs of need and cues of being watched, as well as in the presence of proactive prosociality. We discuss ultimate explanations for these derived features, in particular the adoption of cooperative breeding as well as concern for reputation and costly signalling during human evolution.     

Nongenetic inheritance and the evolution of costly female preference

In species where males provide neither direct benefits nor paternal care, it is typically assumed that female preferences are maintained by indirect selection reflecting genetic benefits to offspring of preferred males. However, it remains unclear whether populations harbour sufficient genetic variation in fitness to support costly female preferences – a problem called the ‘lek paradox’. Here, we ask whether indirect selection on female preferences can be maintained by nongenetic inheritance. We construct a general model that can be used to represent either genetic or nongenetic inheritance, depending on the choice of parameter values. Interestingly, we find that costly preference is most likely to evolve and persist when fitness depends on an environmentally induced factor that can be transmitted over a single generation only, such as an environment‐dependent paternal effect. Costly preference can also be supported when fitness depends on a highly mutable factor that can persist over multiple generations, such as an epigenetic mark, but the necessary conditions are more restrictive. Our findings show that nongenetic inheritance provides a plausible hypothesis for the maintenance of costly female preferences in species where males provide no direct benefits to females. Nongenetic paternal inheritance of fitness can occur in species lacking conventional forms of paternal care. Indeed, transmission of paternal condition via sperm‐borne nongenetic factors may be more likely to evolve than conventional forms of paternal investment because sperm‐borne effects are protected from cuckoldry. Our results furnish a novel example of an interaction between genetic and nongenetic inheritance that can lead to otherwise unexpected evolutionary outcomes.     

A game theoretical approach to the evolution of structured communication codes

Structured meaning-signal mappings, i.e., mappings that preserve neighborhood relationships by associating similar signals with similar meanings, are advantageous in an environment where signals are corrupted by noise and sub-optimal meaning inferences are rewarded as well. The evolution of these mappings, however, cannot be explained within a traditional language evolutionary game scenario in which individuals meet randomly because the evolutionary dynamics is trapped in local maxima that do not reflect the structure of the meaning and signal spaces. Here we use a simple game theoretical model to show analytically that when individuals adopting the same communication code meet more frequently than individuals using different codes—a result of the spatial organization of the population—then advantageous linguistic innovations can spread and take over the population. In addition, we report results of simulations in which an individual can communicate only with its K nearest neighbors and show that the probability that the lineage of a mutant that uses a more efficient communication code becomes fixed decreases exponentially with increasing K. These findings support the mother tongue hypothesis that human language evolved as a communication system used among kin, especially between mothers and offspring.     

Plant signalling: the opportunities and dangers of chemical communication

The notion of chemical communication between plants and other organisms has gone from being viewed as a fringe idea to an accepted ecological phenomenon only recently. An Organized Oral Session at the August 2010 Ecological Society of America meeting in Pittsburgh examined the role of plant signalling both within and between plants, with speakers addressing the remarkably wide array of effects that plant signals have on plant physiology, species interactions and entire communities. In addition to the familiar way that plants communicate with mutualists like pollinators and fruit dispersers through both chemical and visual cues, speakers at this session described how plants communicate with themselves, with each other, with herbivores and with predators of those herbivores. These plant signals create a complex odour web superimposed upon the more classical food web itself, with its own dynamics in the face of exotic species and rapid community assembly and disassembly.     

Modular assembly of genes and the evolution of new functions

Modular assembly of novel genes from existing genes has long been thought to be an important source of evolutionary novelty. Thanks to major advances in genomic studies it has now become clear that this mechanism contributed significantly to the evolution of novel biological functions in different evolutionary lineages. Analyses of completely sequenced bacterial, archaeal and eukaryotic genomes has revealed that modular assembly of novel constituents of various eukaryotic intracellular signalling pathways played a major role in the evolution of eukaryotes. Comparison of the genomes of single-celled eukaryotes, multicellular plants and animals has also shown that the evolution of multicellularity was accompanied by the assembly of numerous novel extracellular matrix proteins and extracellular signalling proteins that are absolutely essential for multicellularity. There is now strong evidence that exon-shuffling played a general role in the assembly of the modular proteins involved in extracellular communications of metazoa. Although some of these proteins seem to be shared by all major groups of metazoa, others are restricted to certain evolutionary lineages. The genomic features of the chordates appear to have favoured intronic recombination as evidenced by the fact that exon-shuffling continued to be a major source of evolutionary novelty during vertebrate evolution.     

Energetic stress and the degree of fluctuating asymmetry: Implications for a long-lasting,honest signal

Summary Duplicate, bilateral structures of individual animals are usually symmetrical. In cases where such structures are asymmetrical, the degree of asymmetry may indicate the propensity of an individual to stray from the genetically programmed outcome during the development of the structure. Asymmetries have recently been assumed to constitute an honest signal of male quality and, as such, a cue for female choice. I tested the assumption that different rates of energy intake would produce differences in the degree of asymmetry by measuring original and induced fourth rectrices of both sides of the body in European nuthatchesSitta europaea. I found no predominance for the right or left side, thus showing the fluctuating nature of the asymmetry at a population level. This was not the case within individuals which consistently had a longer fourth rectrix on one or the other side of the body. Induced rectrices, grown during winter when food availability was relatively low, exhibited a higher degree of asymmetry than did such rectrices grown during winter after hoardable food had been provided earlier during the winter. The original rectrices, grown during relatively benign conditions in late summer, showed the smallest degree of fluctuating asymmetry. This indicates that the degree of asymmetry is affected by the rate of energy intake. Thus, male quality, reflecting the rate with which energy can be secured and shown by differing degrees of asymmetry, can be used as an honest, long-lasting cue by females in their choice of a mate.     

Spatial Dynamics and the Evolution of Enzyme Production

We re-examine the problem of the evolution of protein synthesis or enzyme production using a stochastic cellular automaton model, where the replicators are fixed in the sites of a two-dimensional square lattice. In contrast with the classical chemical kinetics or mean-field predictions, we show that a small colony of mutant, protein-mediated (enzymatic) replicators has an appreciable probability to take over a resident population of simpler, direct-template replicators. In addition, we argue that the threshold phenomenon corresponding to the onset of invasion can be described quantitatively within the physics framework of nonequilibrium phase transitions. We study also the invasion of a resident population of enzymatic replicators by more efficient replicators of the same kind, and show that although slightly more efficient mutants cannot invade, invasion is a likely event if the productivity advantage of the mutants is large. In this sense, the establishment of a population of enzymatic replicators is not a `once-forever' evolutionary decision.     

Patterns of rectrix rachis modification in pintails and the evolution of sexually selected traits

In order to transmit aerodynamic forces to the rest of the body, tail feathers need to be stiff to resist lift forces with minimum deformation. Because delta-wing theory predicts that such feathers do not produce lift forces beyond the point of the maximum continuum width of the tail, species with pintails should not require stiff central rectrices distal to that point. We tested this prediction by comparing the relative thickness of the central rectrix rachis in taxa with pintails and triangular tails. Fourteen pairs of closely related species or species groups belonging to the families Phaethontidae, Phalacrocoracidae, Anatidae, Stercorariidae, Psittacidae, Trochilidae, Alcedinidae, Momotidae, Meropidae, Bucerotidae, Tyrannidae, Pipridae and Nectariniidae were compared. Twelve of the phylogenetically independent comparisons showed that the taxa with triangular tails have higher relative rachis thickness (RRT) than their pintailed relatives just behind the point of the maximum continuum width of the tail. In contrast, two taxa with pintails showed proportionately higher RRT than their triangular-tailed relatives. Triangular tails showed an approximately linear relationship between RRT and relative rachis length, which contrasts with a proportionately greater increase in RRT from distal to proximal parts of the feather in 12 pintailed taxa. These results show that in most of the pintailed taxa studied the distal part of the central rectrix rachis has not been selected to resist lift forces and may be adaptively reduced to attenuate the costs of a hypertrophied ornament. However, the presence of distally reinforced rachices in Eumomota superciliosa and Colonia colonus suggests that a different explanation may be required to account for the design of pintail structure in other taxa.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 477–485.