Social competition affects electric signal plasticity and steroid levels in the gymnotiform fish Brachyhypopomus gauderio

Sexually-selected communication signals can be used by competing males to settle contests without incurring the costs of fighting. Steroid regulation of these signals can render them as reliable indicators of a male's physiological state. We investigated how plasticity in electrocommunication signals is driven by social competition for mates, mediated by steroid hormones, and subject to the effects of past social experience. We measured the electric waveform's amplitude and duration and steroid hormone levels of male gymnotiform electric fish (Brachyhypopomus gauderio) following week-long periods of social isolation, and low or high social competition. To quantify the effect of social history on the modulation of the electric signal, six groups of six males experienced all three social conditions but in different order. We found that males differentially modulate their electric signals depending on the order they experienced these conditions. Thus, past social interactions affect both present and future social electric signals. Cortisol levels and the amplitude of the electric signal appeared to track the intensity of competition, while androgen levels and the duration of the electric signal only responded to the presence (low and high competition) or absence (isolation) of a social environment (low and high androgens respectively). In addition, cortisol levels were related to the body size of the males at high social competition. Taken together, these findings suggest that the capacity of males to modulate their signals in response to social competition is regulated by steroids.     

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.     

Why not lie? Costs enforce honesty in an experimental signalling game

Communication depends on reliability. Yet, the existence of stable honest signalling presents an evolutionary puzzle. Why should animals signal honestly in the face of a conflict of interest? While students of animal signalling have offered several theoretical answers to this puzzle, the most widely studied model, commonly called the ‘handicap principle’, postulates that the costs of signals stabilize honesty. This model is the motivating force behind an enormous research enterprise that explores signal costs—whether they are physiological, immunological, neural, developmental or caloric. While there can be no question that many signals are costly, we lack definitive experimental evidence demonstrating that costs stabilize honesty. This study presents a laboratory signalling game using blue jays (Cyanocitta cristata) that provides, to our knowledge, the first experimental evidence showing honesty persists when costs are high and disappears when costs are low.     

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.     

Breeding density affects the honesty of bird vocal displays as possible indicators of male/territory quality

Vocal displays are supposed to be an honest signal of the phenotypic and genetic quality of individuals and their territory. Moreover, signal interactions are nearly always associated with individuals in aggregations, and their function could in part be explained as social behaviour. Conspecific density has been shown to be a particularly strong proximate and ultimate factor acting on several individual/population features; thus, it may be expected to affect vocal behaviour too. Here, I investigate the hypothesis that, in long‐lived, territorial species, density affects the vocal displays of mated males, masking their honesty as a possible signal of male/territory quality. Each month I listened to the dusk calls of 17 breeding male Eurasian Eagle Owls Bubo bubo during their prelaying period. Nine males bred in a low‐density situation, the other eight in a high‐density one. Conspecific density was found to affect the honesty of call features as signals of male and/or territory quality. The call display as a reliable predictor of male fitness measured as productivity persisted only in situations of high breeding owl density, where male–male competition was stronger. Accommodation of call activity allows individuals to minimize the costs of aggressive calling by adjusting the territoriality threshold to local conditions. The results of this study emphasize the importance, when investigating the evolution and maintenance of honest territorial or sexual signals, of considering the environmental and social context experienced by the individual, thereby corroborating the idea that male–male competition contributes to the maintenance of honest signalling.     

Plasticity in singing effort and its relationship with monoamine metabolism in the songbird telencephalon

Factors intrinsic or extrinsic to individuals, such as their quality or the quality of competition in their social environment, can influence their communication signaling effort. We hypothesized that telencephalic monoamine secretion mediates the effects of a male's own quality and quality of his social environment on his sexual signaling effort. The duration of a male European starling's (Sturnus vulgaris) principal sexual signal, his song, positively correlates with several aspects of his quality, including his reproductive success, immunocompetence, and ability to attract mates. Therefore, the length of songs to which he is exposed reflects, in part, the quality of competition in his social environment. We manipulated the quality of the competitive environment by exposing male starlings to long or short songs for 1 week. We measured the length of songs produced by experimental males to gauge their quality, counted the number of songs they produced to gauge singing effort, and quantified telencephalic monoamine metabolism using high‐pressure liquid chromatography. Singing effort increased with the length of the males' own songs and with the length of songs to which we exposed them. Norepinephrine metabolism in area X of the song control system was negatively correlated with the subjects' mean song length and singing effort. Serotonin metabolism in the caudomedial mesopallium of the auditory telencephalon increased with the length of songs to which we exposed the subjects and with their singing effort. This raises the hypothesis that serotonin and norepinephrine secretion in the telencephalon help mediate the effects of extrinsic and intrinsic factors on signaling effort. © 2009 Wiley Periodicals, Inc. Develop Neurobiol, 2010     

A performance-based cost to honest signalling in male green anole lizards (Anolis carolinensis)

Sexual signals are considered costly to produce and maintain under the handicap paradigm, and the reliability of signals is in turn thought to be maintained by these costs. Although previous studies have investigated the costly nature of signal production, few have considered whether honesty might be maintained not by the costliness of the signal itself, but by the costs involved in producing the signalled trait. If such a trait is itself costly to produce, then the burden of energetic investment may fall disproportionately on that trait, in addition to any costs of signal maintenance that may also be operating. Under limited resource conditions, these costs may therefore be great enough to disrupt an otherwise reliable signal-to-trait relationship. We present experimental evidence showing that dietary restriction decouples the otherwise honest relationship between a signal (dewlap size) and a whole-organism performance trait (bite force) in young adult male Anolis carolinensis lizards. Specifically, while investment in dewlap size is sustained under low-resource condition relative to the high-resource treatment, investment in bite force is substantially lower. Disruption of the otherwise honest dewlap size to bite force relationship is therefore driven by costs associated with the expression of performance rather than the costs of signal production in A. carolinensis.     

Measuring sexual size dimorphism in birds

Vocal displays are supposed to be an honest signal of the phenotypic and genetic quality of individuals and their territory. Moreover, signal interactions are nearly always associated with individuals in aggregations, and their function could in part be explained as social behaviour. Conspecific density has been shown to be a particularly strong proximate and ultimate factor acting on several individual/population features; thus, it may be expected to affect vocal behaviour too. Here, I investigate the hypothesis that, in long-lived, territorial species, density affects the vocal displays of mated males, masking their honesty as a possible signal of male/territory quality. Each month I listened to the dusk calls of 17 breeding male Eurasian Eagle Owls Bubo bubo during their prelaying period. Nine males bred in a low-density situation, the other eight in a high-density one. Conspecific density was found to affect the honesty of call features as signals of male and/or territory quality. The call display as a reliable predictor of male fitness measured as productivity persisted only in situations of high breeding owl density, where male–male competition was stronger. Accommodation of call activity allows individuals to minimize the costs of aggressive calling by adjusting the territoriality threshold to local conditions. The results of this study emphasize the importance, when investigating the evolution and maintenance of honest territorial or sexual signals, of considering the environmental and social context experienced by the individual, thereby corroborating the idea that male–male competition contributes to the maintenance of honest signalling.     

Body postures and patterns as amplifiers of physical condition

The question of why receivers accept a selfish signaller's message as reliable or 'honest' has fuelled ample controversy in discussions of communication. The handicap mechanism is now widely accepted as a potent constraint on cheating. Handicap signals are deemed reliable by their costs: signallers must choose between investing in the signal or in other aspects of fitness. Accordingly, resources allocated to the signal come to reflect the signaller's fitness budget and, on average, cheating is uneconomic. However, that signals may also be deemed reliable by their design, regardless of costs, is not widely appreciated. Here we briefly describe indices and amplifiers, reliable signals that may be essentially cost free. Indices are reliable because they bear a direct association with the signalled quality rather than costs. Amplifiers do not directly provide information about signaller quality, but they facilitate assessment by increasing the apparency of pre-existing cues and signals that are associated with quality. We present results of experiments involving a jumping spider (Plexippus paykulli) to illustrate how amplifiers can facilitate assessment of cues associated with physical condition without invoking the costs required for handicap signalling.     

Increased signalling effort when survival prospects decrease: male-male competition ensures honesty

For signalling to be honest the handicap principle claims that signals must impose fitness costs so that only the best individuals can afford the most exaggerated signals. The cost of signalling in terms of reduced survival decreases, however, towards the end of an individual's lifetime, which can induce an increase in signalling effort as a terminal effort. I show for the three-spined stickleback, Gasterosteus aculeatus, that a decrease in survival prospects through impaired condition leads to an increase in red nuptial coloration that makes the signal less reliable as an indicator of male parental ability. Males in poor condition with a large signal sometimes cannibalized all the eggs they received, probably to start a new breeding cycle with a higher energy reserve. However, the inclusion of socially imposed costs of signalling through male-male competition during courtship increased the honesty of the signal, as some males in poor condition and of poor parental ability decreased their signal expression. Some cheaters still occurred, but the signalling system was honest on average. This implies that socially imposed costs are important in the maintenance of honest sexual signalling. Dishonesty may occur under favourable conditions when the cost of signalling is reduced. This emphasizes the importance of considering the environmental conditions experienced by individuals when investigating the evolution and maintenance of honest sexual signals. Copyright 2000 The Association for the Study of Animal Behaviour.     

Resource value and the context dependence of receiver behaviour

Many animals use signals of fighting ability to minimize the costs of competition. Theory predicts that signals must be costly to remain reliable indicators of their bearer's abilities, but many signals of fighting ability lack obvious developmental costs. Instead, receivers are thought to maintain signal accuracy by behaving aggressively towards individuals with inaccurate signals (i.e. social costs). Models predict that the evolutionary stability of social cost signals depends on receivers trusting signals in certain contexts and testing signal accuracy in other contexts. Here, I use the signals of agonistic ability in Polistes dominulus wasps to provide the first experimental evidence that receiver responses to social cost signals are context dependent. During contests over low-value resources, wasps trust signals; they avoid patches of food guarded by rivals with elaborate signals. As the value of the resource increases, wasps become more likely to test signal accuracy. In fact, receivers challenge guards regardless of their signal phenotype when the resource is sufficiently valuable. Context-dependent receiver responses are likely to be an important behavioural mechanism underlying the evolution of social costs, as context-dependent responses allow receivers to minimize the costs of conflict while also ensuring signal accuracy.     

The Oxidative Cost of Acoustic Signals: Examining Steroid Versus Aerobic Activity Hypotheses in a Wild Bird

Vertebrate vocalizations are widespread secondary sexual signals used for mate attraction and territory defence, and variation in signal quality is often condition dependent and impacts reproductive outcomes. Although vocal signal performance is known to reflect various aspects of male quality, few studies have examined the underlying mechanisms mediating its costs and hence its honesty. Using a population of Arctic‐breeding snow buntings (Plectrophenax nivalis), we compared the ‘Oxidation Handicap Hypothesis’, which predicts that testosterone‐induced increases in oxidative stress provide a direct mechanistic basis for ensuring the honesty of many secondary sexual signals, to the ‘Aerobic Activity Hypothesis, which predicts that it is the aerobic activity involved with signal production (i.e. vocal performance or defending a large territory) and not testosterone directly that links signal quality and oxidative stress. Males singing at faster rates had higher levels of both reactive oxygen metabolites and non‐enzymatic antioxidant capacity in the plasma (i.e. without an increase in overall oxidative stress), enabling certain males to produce high‐quality signals while also mitigating the costs of an associated increase in oxidative stress. However, these results were completely independent of plasma testosterone levels, supporting the role of aerobic performance in directly affecting oxidative stress. Although song performance was not linked to reproductive parameters in our data set, our research is the first to test these competing hypotheses in a behavioural trait and results suggest that oxidative stress may be an underlying physiological cost preventing low‐quality individuals from producing high‐quality signals.     

The cost of dishonesty

The handicap principle states that stable biological signals must be honest and costly to produce. The cost of the signal should reflect the true quality of the signaller. Here, it is argued that honest signalling may be maintained although the used signals are not handicaps. A game theoretic model in the form of a game of signalling is presented: all the existing evolutionarily stable strategies (ESSs) are found. Honest and cheap signalling of male quality is shown to be evolutionarily stable if females divorce the mate if it turns out that he has cheated about his quality. However, for this ESS to apply, the cost of lost time must not be too great. The stability of the honest signalling is based on deceivers being prevented from spreading in the population because they suffer from a cost of divorce. Under some fairly strict conditions, a mixed polymorphism of dishonesty and honesty represents another possible ESS.     

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

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

The 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.     

CONSPIRATORIAL WHISPERS AND CONSPICUOUS DISPLAYS: GAMES OF SIGNAL DETECTION

Recent models of signaling have assumed that the expenditure required to ensure detection of a display is negligible and have concentrated instead on the costs that may be necessary to maintain honesty. Such models predict that individuals who share the same interests are likely to communicate using “conspiratorial whispers,” signals that are cheap and inconspicuous. Here, I present a game-theoretical model of signal detection (in a noisy environment, in the presence of potential eavesdroppers), which demonstrates that the idea of conspiratorial whispers is far too simplistic. It is true that in “cooperative” signaling systems (where signalers attempt to elicit responses that are beneficial for receivers), signal cost is not required to maintain honesty. However, some level of expenditure is still needed to ensure that a signal is reliably detected. Moreover, there exists a conflict of interest between signalers and receivers over the division of this expenditure. To predict the stable level of display in such cases, one needs to know how this conflict of interest will be resolved. The model reveals that the outcome may range from a whisper to a conspicuous and costly (though still conspiratorial) display. The more closely related the receiver is to the signaler, the greater the level of signal exaggeration that is expected—the opposite prediction to that of honest signaling models.     

Birds' tails as signaling devices: markings, shape, length, and feather quality

While exaggerated length and ornamental shapes are confirmed sexually selected tail traits in birds, the signal function of tail markings has received less study. Signal roles for tail markings as amplifiers of length, shape, and feather quality are discussed, and the role of tail markings as feather-quality handicaps is proposed: absence of melanin increases damage and abrasion. Predicted correlations of tail markings with other tail traits are derived for these signal roles. A comparative study of the relationships between these tail traits in an entire avifauna, the western Palearctic, tested the predictions. Tail displays were present in nearly 80% of species, associated with greater long-tailedness, but not all displayed tails had markings or ornamental shape. The incidence of marks across tail shapes and the combinations of marks indicate that tail markings act as handicaps or amplifying handicaps of tail feather quality. Tail elongation and ornamental shapes could act as additional handicaps of feather quality-that is, they could be multipurpose signals. Incorporation of revealing indicators such as feather damage and associated handicap and/or amplifying traits may allow a reduction in the cost of signaling while maintaining signal reliability and, hence, influence sexual selection in complex signaling systems.     

The truthful signalling hypothesis: an explicit general equilibrium model

In mating competition, the truthful signalling hypothesis (TSH), sometimes known as the handicap principle, asserts that higher-quality males signal while lower-quality males do not (or else emit smaller signals). Also, the signals are "believed", that is, females mate preferentially with higher-signalling males. Our analysis employs specific functional forms to generate analytic solutions and numerical simulations that illuminate the conditions needed to validate the TSH. Analytic innovations include: (1) A Mating Success Function indicates how female mating choices respond to higher and lower signalling levels. (2) A congestion function rules out corner solutions in which females would mate exclusively with higher-quality males. (3) A Malthusian condition determines equilibrium population size as related to per-capita resource availability. Equilibria validating the TSH are achieved over a wide range of parameters, though not universally. For TSH equilibria it is not strictly necessary that the high-quality males have an advantage in terms of lower per-unit signalling costs, but a cost difference in favor of the low-quality males cannot be too great if a TSH equilibrium is to persist. And although the literature has paid less attention to these points, TSH equilibria may also fail if: the quality disparity among males is too great, or the proportion of high-quality males in the population is too large, or if the congestion effect is too weak. Signalling being unprofitable in aggregate, it can take off from a no-signalling equilibrium only if the trait used for signalling is not initially a handicap, but instead is functionally useful at low levels. Selection for this trait sets in motion a bandwagon, whereby the initially useful indicator is pushed by male-male competition into the domain where it does indeed become a handicap.     

Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird

Sexual displays often involve several different ornamental traits. Yet most indicator models of sexual selection based on a single receiver (usually a choosy female) find that multiple handicap signals should be unstable. Here we study reasons for this contradiction, analyzing signal function, signal content, and trade-offs between signals in the polygynous red-collared widowbird Euplectes ardens. Males have both a long, graduated tail and a red carotenoid collar badge. Territory-holding "residents" have slightly shorter tails than the nonbreeding "floaters," but their carotenoid collars are 40% larger, and they have (on the basis of reflectance spectrometry and objective colorimetry) a 23-nm more long-wave ("redder") hue than floaters. This corroborates experimental evidence that the red collar is selected by male contest competition, whereas female choice is based almost exclusively on male tail length. Tail length is negatively correlated with the carotenoid signal, which together with body size and condition explains 55% of the variation in tail length. The trade-off in tail length and carotenoid investment is steeper among residents, suggesting an interaction with costs of territory defense. We propose that the "multiple receiver hypothesis" can explain the coexistence of multiple handicap signals. Furthermore, the trade-off between signal expressions might contribute to the inverse relation between nuptial tail elongation and coloration in the genus Euplectes (bishops and widowbirds).     

The dynamics of honesty: modelling the growth of costly, sexually-selected ornaments

The handicap principle suggests that individuals of superior quality can more easily bear the cost of developing extravagant ornaments. Consequently, ornament size should provide reliable information about quality or condition. Previous models have largely ignored the process of ornament growth, focusing only on final ornament size. We model ornament growth schedules for individuals of different qualities, where higher quality individuals experience lower costs of carrying energy reserves of a given size, but where all individuals pay a net cost of carrying ornaments of a given size. If the costs of ornament production ensure that final ornament size reliably signals quality, the information conveyed by the signal can change dramatically during growth. Higher quality individuals should delay growth until closer to breeding. Taking a snapshot of partially developed ornaments prior to breeding would show them to be larger in poorer quality individuals. The claim that costly ornaments honestly signal quality thus needs to be understood in a dynamic context, and may only hold during some phases of growth.