Honesty of a dynamic female aggressive status signal: baseline testosterone relates to bill color in female American goldfinches

Status signals are linked to fighting ability and enable competitors to gain access to resources without risking injury in aggressive combat. The relationship between testosterone (T), a hormone that mediates aggression, and signals of status is well studied in males, but little is known about the relationship between T and female signals of status. Female and male American goldfinches Spinus tristis express a dynamic carotenoid‐based orange bill color during the breeding season and previous work has demonstrated that females use orange bill color to communicate competitive ability during intrasexual competition. We test the hypothesis that female bill color reflects baseline T, which would allow receivers to directly assess a competitor's aggressive potential. We found a positive relationship between T and bill coloration in females, indicating that bill color has the ability to signal female competitive status. This finding is consistent with the hypothesis that female bill color is a reliable signal of fighting ability, and indicates that females, like males, may use coloration to signal their hormonally mediated aggressive potential.     

Weaponry, color, and contest success in the jumping spider Lyssomanes viridis

Weaponry and color badges are commonly theorized to function as visual signals of aggressiveness or fighting ability. However, few studies have supported a signaling function of weaponry, and the role of color in invertebrate competitive interactions remains virtually unexplored. Jumping spiders (Salticidae) make excellent invertebrate models for studying weaponry and color because males of many species are colorful and possess exaggerated chelicerae, which are used as weapons in escalated contests. To determine whether color or weaponry might function as visual signals in male-male competitions, we investigated relationships between contest success, cheliceral length, and red coloration in Lyssomanes viridis. Males having longer chelicerae than their opponents were significantly more likely to win (p=0.0008). Males who won, despite being smaller than their opponents, had significantly less red chelicerae than their opponents (p=0.01). Male and female cheliceral length, as well as foreleg length, correlated tightly with body size. Cheliceral and foreleg length showed significantly stronger positive allometry in males than in females. We conclude that male chelicerae and forelegs are under strong positive selection for their use in physical fights and/or as visual signals of fighting ability.     

Is Brightest Best? Testing the Hamilton-Zuk Hypothesis in Mandrills

Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here, we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle), immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability (MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions for future studies on the signal content of color in mandrills and other primates.     

Social correlates of testosterone and ornamentation in male mandrills

We investigated relationships between fecal androgen concentrations, facial coloration and behaviour in semi-free-ranging male mandrills. We found that fecal androgen levels were significantly positively related to dominance rank, independent of rank stability and the mating period, suggesting that male mandrills live in a permanently aggressive context in which they must actively maintain their dominance status. Facial red coloration was also significantly related to both fecal androgen levels and rank, with high ranking males having both higher androgen levels and redder faces, although dominant males did not always have the highest androgen levels or the reddest faces. Predictive relationships between androgen levels, coloration and rank were short-term. Androgen concentrations and facial redness both increased in the presence of receptive females, as did the former during periods of rank instability. We conclude that male facial redness is likely to represent an honest signal (to other males) of current androgen status, competitive ability and willingness to engage in fights and that females may also use this to assess male condition. Further, our findings provide support for the “challenge hypothesis” as originally proposed for birds by Wingfield.     

Do Female Mandrills Prefer Brightly Colored Males?

Although secondary sexual adornments are widespread in male primates, few studies have examined female choice for these characters. Mandrills (Mandrillus sphinx) present an extreme example of sexual dimorphism, with males exhibiting an array of striking adornments. The most dominant adult male in a group exhibits the brightest and most extensive red coloration, while the other males are less brightly colored. I examined whether female mandrills prefer brightly colored males using data on periovulatory sexual behavior during the 1996 mating season for all males 8 years old (n = 5) and all parous females (n = 9) in a semifree-ranging colony at CIRMF, Gabon. Brightness of male coloration is significantly positively correlated with time spent within 2 m of females, female responsibility for proximity, number of sexual presentations received, % approaches accepted by females, and % inspections with which females cooperated. Females also groomed only the brightest male. Behaviors indicating female preference are not correlated significantly with male dominance rank, and partial correlations confirm that the influence of male color on female behavior is stronger than that of male rank. With the influence of male dominance rank controlled, correlation coefficients between female behaviors and male mating success are high and positive. In further support of the hypothesis that females show mate choice for brightly colored males, independent of dominance rank, I report an unusual case wherein the alpha male fell in rank without loss of coloration. He experienced no significant change in female responsibility for proximity, sexual presentations received, or female reaction to approaches or inspections, though he was no longer observed to mate. Accordingly, female mandrills attend to differences in male secondary sexual characters and favor brightly colored males. As brightly colored males are also dominant this reinforces the influence of male-male competition on male reproductive success and may explain the very high reproductive skew in mandrill males and their extraordinary appearance.     

The role of pigment based plumage traits in resolving conflicts

The role of melanin ‘badges of status’, in male–male competition has been well‐studied, in contrast, carotenoid based plumage has largely been examined in the context of female mate choice. Recent work has shown that carotenoid signals can also function in male–male competition, although the functions of the two types of signals is currently unclear. Here, we examine the relationships between colouration, dominance and aggression in the crimson finch Neochmia phaeton, a species where males have both conspicuous red carotenoid plumage and a black melanin patch. We examined the importance of carotenoid and melanin based signals in three contexts: 1) among free‐living birds interacting at a feeding station: we found that neither colour signal influenced the outcome of interactions; 2) in staged dyadic contest in captivity: we found that coloration from carotenoid pigments was positively related to the probability of winning a contest, while the size of the melanin plumage patch was not related to winning; and 3) in staged dyadic contests where male plumage colour had been masked: we found that the number of interactions required to determine dominance increased. While the underlying natural plumage colour was still important in these contests, birds with more intense carotenoid colouration were now more likely to lose. These results confirm carotenoid‐based signalling in male–male contests. However this signal is used in conjunction with other factors such as self‐assessment and body condition. Contrary to traditional expectations, the black melanin patch was not found to be important in this context.     

Red clothing increases perceived dominance,aggression and anger

The presence and intensity of red coloration correlate with male dominance and testosterone in a variety of animal species, and even artificial red stimuli can influence dominance interactions. In humans, red stimuli are perceived as more threatening and dominant than other colours, and wearing red increases the probability of winning sporting contests. We investigated whether red clothing biases the perception of aggression and dominance outside of competitive settings, and whether red influences decoding of emotional expressions. Participants rated digitally manipulated images of men for aggression and dominance and categorized the emotional state of these stimuli. Men were rated as more aggressive and more dominant when presented in red than when presented in either blue or grey. The effect on perceived aggression was found for male and female raters, but only male raters were sensitive to red as a signal of dominance. In a categorization test, images were significantly more often categorized as ‘angry’ when presented in the red condition, demonstrating that colour stimuli affect perceptions of emotions. This suggests that the colour red may be a cue used to predict propensity for dominance and aggression in human males.     

Repeated Recent Aggressive Encounters Do Not Affect Behavioral Consistency in Male Siamese Fighting Fish

Consistent individual differences in behavior suggest that individuals respond in a predictable and repeatable manner in a specific situation while differing from other individuals. Male Siamese fighting fish exhibit consistent individual differences in decision‐making strategies when they encounter a receptive female and a rival male simultaneously. However, whether these differences are altered by recent experience is unknown. We examined the influence of repeated aggressive encounters on behavioral consistency and decision‐making. Males were presented with paired female–male dummies prior to any aggressive experiences to obtain a baseline measure. Next, males either won or lost three consecutive contests against rivals and then received the paired female–male dummies after each of these encounters. Overall levels of highly aggressive behaviors were affected by contest outcome, while levels of female‐directed were not. Not surprisingly, winning a fight led to an increase in male‐directed bites, an overtly aggressive behavior that only occurs after fights have escalated. Fighting a male before encountering the dummies caused males to perform more tail beats to the dummy male, perhaps as a result of increased motivation. Males exhibited similar levels of repeatability and used the same strategies when faced with conflicting stimuli regardless of fighting experience. Thus, while winning or losing a fight impacts overall aggression, it does not influence behavioral consistency. This study demonstrates that consistent individual differences and decision‐making strategies may be resistant to recent aggressive experiences, even over a period of days.     

Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics

Instances of bright, hormonally induced coloration among females during gestation have been reported in a few reptile and primate genera. Gravid coloration in lizards has been linked to female aggression but the influence of color changes associated with pregnancy has not yet been experimentally pursued for primates. As a first step to determine whether the crimson to magenta hues common to pregnancy coloration in rhesus macaques (Macaca mulatta) contains information, to which conspecifics of either sex attend, we evaluated whether male and female rhesus macaques discriminate between pregnant and non-pregnant female faces. To these ends, we presented 19 adult rhesus macaques with color-manipulated digital images of female faces where pregnancy coloration was present or absent, and measured visual attention and behavioral reactions. Males were significantly more attentive to female faces with pregnancy coloration over those without pregnancy coloration. Both sexes engaged in higher levels of appeasement behavior toward stimulus with pregnancy coloration, and males showing signs of anxiety did so exclusively when exposed to faces with pregnancy coloration. Our results suggest that pregnancy coloration might be an attention grabbing stimulus to males and a warning stimulus to both male and female rhesus macaques. The findings provide a comparative perspective on the use of color in intra-specific communication, and suggest similarity in female similarity in signalling properties in distantly related taxa.     

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

A broad range of animals use visual signals to assess potential mates, and the theory of sensory exploitation suggests variation in visual systems drives mate preference variation due to sensory bias. Trinidadian guppies (Poecilia reticulata), a classic system for studies of the evolution of female mate choice, provide a unique opportunity to test this theory by looking for covariation in visual tuning, light environment and mate preferences. Female preference co‐evolves with male coloration, such that guppy females from ‘low‐predation’ environments have stronger preferences for males with more orange/red coloration than do females from ‘high‐predation’ environments. Here, we show that colour vision also varies across populations, with ‘low’‐predation guppies investing more of their colour vision to detect red/orange coloration. In independently colonized watersheds, guppies expressed higher levels of both LWS‐1 and LWS‐3 (the most abundant LWS opsins) in ‘low‐predation’ populations than ‘high‐predation’ populations at a time that corresponds to differences in cone cell abundance. We also observed that the frequency of a coding polymorphism differed between high‐ and low‐predation populations. Together, this shows that the variation underlying preference could be explained by simple changes in expression and coding of opsins, providing important candidate genes to investigate the genetic basis of female preference variation in this model system.     

Aggression Levels Affect Social Interaction in the Non‐Breeding Territorial Aggression of the Weakly Electric Fish,Gymnotus omarorum

Animals typically decide whether to fight or retreat from conspecifics based on their individual estimates of the costs and benefits of fighting. Theoretical models predict how contenders solve a conflict, but the evaluation processes involved in these decisions depend on multiple factors that are difficult to explore experimentally. We addressed these questions using the non‐breeding territorial aggression of Gymnotus omarorum, in which subordinates make three distinctive decisions to signal their submission during a fight: (1) interruption of their electric discharges to hide from the dominant, (2) stop attacking and retreat, and (3) emission of ‘chirps’, transient submissive electric signals. We confirmed that subordinates take into account the aggressive performance of dominants to shape their own agonistic decisions and performance. The intensity of aggression is highly correlated with an agonistic dyad, and the decision of subordinates to retreat is influenced by the attack rates of dominants. When we lowered the aggression of expected dominants with a 5‐HT_1A receptor agonist, the correlation between the two contenders' aggression levels was lost and subordinates completely stopped emitting electric chirp signals. The aforementioned results contribute to the understanding of the decision‐making strategies driven by social challenge inherent to agonistic encounters.     

Parental care and UV coloration in blue tits: opposite correlations in males and females between provisioning rate and mate’s coloration

Parental investment and sexually‐selected signals can be intimately related, either because the signals indicate the amount of investment that an individual is prepared to make, and hence its value as a mate (the ‘good parent process’), or because individuals are selected to vary their own investment in relation to their mate’s signals (‘differential allocation’ or ‘reproductive compensation’). Correlations between parental investment and the sexually selected signals of both an individual and its mate are therefore of central interest in sexual selection. Blue tits Cyanistes caeruleus are an ideal study species to investigate such correlations because they provide substantial amounts of biparental care and possess sexually‐selected structural UV coloration that seems to signal attractiveness in both sexes. We investigated whether feeding rates of male and female blue tits were correlated with either their own or their mate’s UV coloration, and whether any such correlation was affected by the sex ratio of the brood. We also investigated whether any such correlations were reflected in offspring phenotype. Feeding rates were not correlated with either sex of parent’s own UV coloration. However, they were correlated with the mate’s UV coloration, but in opposite directions in males and females: females had higher feeding rates when mated to bright UV males, implying differential allocation, while males had lower feeding rates when mated to bright UV females, implying reproductive compensation. These relationships were unaffected by the sex ratio of the brood. In addition, fledgling tarsus length, but not mass, was related to male UV coloration, and to female UV coloration in interaction with male age. These results suggest that both male and female attractiveness influence parental investment of the mate, and that this in turn affects offspring phenotype. We found no evidence for differential sex allocation.     

Mate Preference for Novel Phenotypes: A Fresh Face Matters

Conspicuous polymorphism in sexually selected traits is usually attributed to processes such as frequency‐dependent selection that can maintain genetic variation. Recent evidence indicates that dramatic variation of male coloration in guppies (Poecilia reticulata) is promoted by a form of frequency‐dependent selection in which males bearing rare or novel color patterns achieve higher mating success than males bearing common patterns. Active female preference for unfamiliar or rare color patterns has been implicated in generating this rare‐phenotype advantage, but the behavioral processes responsible for the preference remain unclear. To determine whether familiarity that is developed over a very short timescale can lead to a rare‐male mating advantage, we measured female response to courtship by males with color patterns that were the same as or different from that of the previous male to court. Females showed two types of short‐term preference variation in this experiment. On the first trial day, females shifted their preferences on a timescale of minutes, showing strong preference for males bearing a color pattern different from that of the immediately previous male to court. Twenty‐four hours later, females were less responsive to male courtship overall, and there was no difference in females’ response to different‐ and same‐morph males. Females also preferred males with more orange coloration on both trial days, but this color preference was independent of the preference for ‘different’ color patterns. These data suggest that the behavioral process underlying rare‐male advantage in guppies is that females prefer males bearing unfamiliar color patterns and that familiarity is determined over a very short timescale.     

Absence of Mate Guarding in the Yellowhammer (Emberiza citrinella)?

The mate guarding behaviour of male yellowhammer (Emberiza citrinella) was studied with special reference to the effects of age, body size (tarsus length) and coloration of males. Measurements of intra-pair distance do at the most provide evidence for relatively lax mate guarding. On the other hand, patterns of male song activity and inter-male aggression were more in agreement with the predictions of the mate guarding hypothesis. The reasons for the comparatively low mate guarding intensity in the yellowhammer may be that males do not need to guard their mates intensely. Age differences were found in song and aggressive activity, older males singing and fighting the most. Size had no effect on guarding behaviour. Coloration was correlated with inter-male aggressiveness and conflict initiation propensity. Less colourful males fought the most in the pre-fertile period of their mates, whereas colourful and old males fought the most during the fertile period. This suggests that coloration may be an indicator of individual fighting and guarding ability.     

Morphological and Behavioural Traits Affecting the Intensity and Outcome of Male Contests in Gallotia galloti galloti (Family Lacertidae)

This study describes the sequence of behaviour during aggressive encounters between male ‘tizón’ lizards (G. galloti galloti) and assesses the effect of morphological and behavioural traits on the outcome and intensity of staged aggressive encounters between males. Aggressive encounters ranged from only throat extension to escalated fights with biting and rolling over. Winners were heavier, had longer heads, and performed tongue-flicking, throat extension and biting at a higher rate than losers. The rate of aggressive behaviour increased with decreasing difference in snout-to-vent length, head length and head width of the contestants. The results are in agreement with some predictions of the sequential assessment game model in that probability of victory increased with the difference in fighting ability and that the rate of aggressive behaviour was higher in contests between animals of similar size.     

Stickleback Males Increase Red Coloration and Courtship Behaviours in the Presence of a Competitive Rival

In species where females preferentially select the most colourful males, males may strategically invest in courtship and nuptial colour according to the presence of rivals. In this experimental study, we tested this in the three‐spined stickleback (Gasterosteus aculeatus) in which mature males exhibit carotenoid‐based red coloration to attract mates and defend their territories against male competitors. We challenged experimental males with either a red‐ornamented dummy male or a non‐ornamented dummy for five min per day in six‐d experimental trial, which was repeated twice during the breeding season. We found that the males presented with a coloured rival exhibited more frequent courtship behaviours (i.e. fanning and gluing) to females than those presented with a non‐coloured intruder during the second experimental trial. At the end of each trial, the experimental males also showed a significantly larger area of red coloration in the presence of a coloured intruder. Our findings suggest that male sticklebacks regulate mating effort according to the presence of competitive rivals by increasing their investment in costly signals when successful mating and territory defence is at risk.     

Carotenoid status signaling in captive and wild red-collared widowbirds: independent effects of badge size and color

Carotenoid-based plumage ornaments are typically consideredto be sexually selected traits, functioning as honest condition-dependentsignals of phenotypic quality, but few studies have addressedthe function of carotenoid color variation in male contestcompetition. Using two experiments, we investigated the statussignaling function of the variable (ranging from yellow tored) carotenoid throat patch (collar) in the polygynous, sexually dimorphic red-collared widowbird (Euplectes ardens). First,we tested if the red collar functions as a dominance signalby painting spectrometrically controlled collar patches ontothe brown plumage of nonbreeding males and staging dyadic malecontests over food resources. Red-collared males dominatedorange males, which in turn dominated the control brown andnovel blue collars. Red dominance persisted when the collar manipulations were reversed within dyads and also when testedagainst testosterone implanted males. In the second experimentthe collar size and color of breeding males were manipulatedin the field before and after territories were established.All males with enlarged red and most with enlarged orange orreduced red collars obtained territories, whereas most maleswith reduced orange and all with blackened (removed) collarsfailed to establish or retain territories. In addition, amongthe territorial males, those with reduced signals defendedsmaller territories, received more intrusions, and spent moretime in aggressive interactions. Redness and, to a lesser extent,size of the carotenoid ornament both seem to independently indicate male dominance status or fighting ability in male contest competition.     

Let's Call A Truce…For Now: The Silent Bared‐Teeth Face Expression in Mandrills (Mandrillus sphinx) During Baseline and Post‐Conflict Conditions

The distinction between signals that are friendly and those that are non‐aggressive but motivationally neutral (signals of benign intent, SBIs) has not often been well elucidated in the literature. Although both signals occur in similar contexts, friendly signals should be exchanged more often between animals with good relationships whereas SBIs should be more commonly exchanged between animals with poor or unpredictable relationships. The importance of this distinction is particularly salient in the post‐conflict context, because the two different types of signals may have disparate distributions and functions. This study examines the nature of the silent bared‐teeth face (SBTF) in captive mandrills (Mandrillus sphinx) both during baseline interactions and following aggressive conflicts. We report that the SBTF is most commonly exchanged between mandrills with high rates of agonism. In addition, the SBTF is the most common post‐conflict signal exchanged, and the mandrills exchanging this signal after fighting also have poor relationships. We conclude that, although one must be careful in generalizing from studies of captive populations, the mandrill SBTF observed in this study is most accurately classified as a signal of benign intent, but not a truly friendly signal and discuss problems with interpreting post‐conflict data without distinguishing between these types of signals.     

Does signalling mitigate the cost of agonistic interactions? A test in a cricket that has lost its song

Prevailing models of animal communication assume that signalling during aggressive conflict mitigates the costs of fighting. We tested this assumption by staging dyadic encounters between male field crickets, Teleogryllus oceanicus, under three conditions: (i) both males could sing aggressive songs, (ii) neither male could sing, and (iii) one male could sing but the other could not. We conducted experiments on males from a Hawaiian population from Kauai that has recently evolved signal loss, and males from a Hawaiian population from the Big Island that has not. Among both populations, interactions between two silent males were characterized by higher levels of aggression than interactions involving one or two singing males. Because the level of aggression is strongly related to the cost of fighting, these data demonstrate that signalling mitigates the cost of fighting. In mixed trials, we found no statistically significant differences between the behaviour of calling and non-calling males in either population. We conclude that there is no evidence that the Kauai population exhibits special adaptations to alleviate the costs of signal loss. Finally, we found that males were much more likely to signal after their opponent''s retreat than after their own retreat. Aggressive song therefore meets the definition of a ‘victory display’.     

Is the parallel walk between competing male fallow deer, Dama dama, a lateral display of individual quality?

During competitive encounters protagonists are expected to use signals of individual quality particularly if there is a risk of injury or death. Lateral presentation of body profile, by which information regarding phenotypic characteristics associated with individual quality are displayed, may represent such a strategy. During aggressive interactions, male fallow deer frequently engage in parallel walking which is assumed to represent a mutual display of quality, as mediated by exposure of the maximal profile of the body or antlers. We examined the context and role of the parallel walk during competitive encounters to investigate whether there was evidence that dyads of competing males were assessing differences in phenotypic characteristics. There was no evidence to support the hypotheses that the parallel walk is a lateral display of body size or weaponry or that its use is associated with a reduced level of escalated or risky behaviours during fighting. Total time spent fighting was not shorter when a parallel walk was present than when there was no parallel walk. The parallel walk was highly associated with fighting and it was more likely to be initiated by the subsequent loser. Furthermore, parallel walking frequently followed bouts of fighting and as such may represent a strategy that permits an animal the opportunity to decide whether to continue fighting. Parallel walking was also associated with a failure to resolve contests in favour of one animal indicating that it may be a means of withdrawing from further fighting without incurring a loss in dominance status. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.