Size of ornament is negatively correlated with baseline corticosterone in males of a socially monogamous colonial seabird

The Goymann–Wingfield model predicts that glucocorticoid levels in social animals reflect the costs of acquiring and maintaining social status. The crested auklet is one of the few avian colonial species where a mutual ornament in males and females is used in both sexual and aggressive displays. Previous studies of the crested auklet support the notion that the crest ornament is a badge of status in this species. Here, we examined the relationship between the crest ornament size and the adrenocortical function in breeding crested auklets. Crest length was negatively correlated with corticosterone at baseline in males, but not in females. Baseline corticosterone in females (but not in males) was negatively correlated with body condition index. Although male and female crested auklets are monomorphic in their ornamental traits, our results suggest that the socially mediated physiological costs associated with status signaling may differ between the sexes.     

Social Control and Physiological Cost of Cheating in Status Signalling Male House Sparrows (Passer domesticus)

Flock-forming passerines often use plumage characteristics to signal their social dominance. While the benefits to signal dominance seem obvious, costs associated with status signalling are ambiguous. The social control hypothesis predicts that individuals of high social status – with large badges – are involved in more social interactions with individuals of similar badge size. Cheaters are therefore exposed to increased risk of fighting with high quality individuals and the costs associated with enhanced fights with dominant males are supposed to outweigh the benefits of cheating. We tested the social control hypothesis in male house sparrows ( Passer domesticus ), by observing social interactions in captive flocks and determining dominance relationships. Two low status individuals within each flock had the size of their badge experimentally increased and the interactions involving experimental and control birds were recorded. We also assessed the potential physiological cost of cheating in terms of enhanced levels of the stress hormone, corticosterone. Dominance was significantly positively correlated with badge size, but not with other morphological traits. We found little support for the social control hypothesis. Birds did not have significantly more interactions with individuals of similar badge size, before the manipulation. Similarly, after the experimental increase in badge size, experimental birds did not tend to have more encounters with large-badged males. Experimental birds with enlarged badges won more fights compared with prior to the manipulation, suggesting that badge size is used as a signal of social dominance even in small and stable flocks. Finally, corticosterone levels in the blood did not increase significantly after the manipulation of badge size, suggesting that there is no measurable cost, resulting from stress, in cheaters.     

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.     

Colourful male European Serins Serinus serinus are more careful with their plumage

Ornamental traits typically advertise individual condition and can be costly to maintain. Plumage maintenance behaviour can increase plumage quality and positively influence female mate preference. We investigated this prediction by performing female mate‐choice trials and measuring male plumage maintenance behaviour in the European Serin Serinus serinus. More colourful males spent more time in plumage maintenance than less colourful males, but this was not correlated with body condition or ectoparasite load. Females preferred more colourful males, although this was not influenced by male plumage maintenance. Our findings highlight the fact that investment in plumage maintenance depends on individual coloration and this may reinforce the honesty of ornamental plumage and convey positive information for mate choice.     

Different Reproductive Tactics in House Sparrows Signalled by Badge Size: Is There a Benefit to Being Average?

Sexual selection models usually predict directional selection for ornamental traits because of intra‐ as well as inter‐sexual selection. Animals frequently face reproductive trade‐offs, such as between mating and parental effort. Provided that both are essential and have opposite effects on ornament expression, we may however not necessarily expect directional selection for ornament size. The house sparrow is an ideal species to study such a trade‐off, as the size of the male ornament, the black throat badge, seems to be inversely related to mating and parental effort. It has been suggested that large‐badged males invest more in female attraction and territory defence, while small‐badged males may invest more in parental care. In a nest‐box study, we show that females started to breed earliest and produced the largest clutches when mated to males with average‐sized badges that invested in paternal care more than other males. These results are discussed in view of inter‐ as well intra‐sexual selection. Overall, average‐badged males experienced the highest hatching failures, their chicks were in the poorest physical condition and they did not fledge more chicks than other males. It is therefore unlikely that the mating advantages that we observed could by themselves lead to stabilizing selection for badge size. Our results rather suggest that badge size in male house sparrows signals different reproductive tactics, which are adapted flexibly according to their physical condition and socio‐ecological situations.     

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.     

Sex‐specific density‐dependent secretion of glucocorticoids in lizards: insights from laboratory and field experiments

Negative density feedbacks have been extensively described in animal species and involve both consumptive (i.e. trophic interactions) and non‐consumptive (i.e. social interactions) mechanisms. Glucocorticoids are a major component of the physiological stress response and homeostasis, and therefore make a good candidate for proximate determinants of negative density feedbacks. Here, we combined laboratory and field experiments with enclosed populations to investigate the relationship between density, social stress and plasma corticosterone levels in the common lizard Zootoca vivipara. This species exhibits strong negative density feedbacks that affect females more than males, and its life history is sensitive to experimentally‐induced chronic elevation of corticosterone plasma levels. We found that prolonged crowding in the laboratory can trigger a chronic secretion of corticosterone independent from food restriction. In the field experiments, corticosterone levels of females were not affected by population density. Corticosterone levels of males increased with population density but only during the late activity season in a first field experiment where we manipulated density. They also increased with density during the mating season but only in populations with a female‐biased sex ratio in a second field experiment where we crossed manipulated density and adult sex ratio. Altogether, our results provide limited evidence for a role of basal corticosterone secretion in density feedbacks in this species. Context and density‐dependent effects in males may arise from changes in behavior caused by competition for resources, male–male competition, and mating.     

Honest signalling,dominance hierarchies and body condition in House Sparrows Passer domesticus (Aves: Passeriformes) during acute coccidiosis

Parasitic infections may change the equilibrium between the costs and benefits of an animal for maintaining its status in a social group. Consequently, parasites may influence the social status of an animal in a group. The present study investigated whether acute infection with Isospora spp. has any effect on the social relationships (e.g. dominance hierarchy) of male house sparrows and how the infection influences their behaviour, immune status, and body condition. Furthermore, the study allowed us to examine how important the ‘badge of dominance’ is with respect to maintaining social status even when the actual condition is changing as a result of infection. The results obtained showed that an acute infection leads to changes in the dominance hierarchy of a social group and that body mass losses of birds depend on the achieved hierarchy status. A positive correlation between the badge size and male aggressiveness was only found during acute infection. In addition, we also found a relationship between cell‐mediated immune response and male aggressiveness during acute infection. This suggests that male badge size is not sufficient to maintain a given dominance position. On the other hand, badge size, a signal developed during the moult, appears to remain an informative and ‘honest’ signal several months later, reflecting the energy reserves of a bird faced with a demanding stressful situation such as acute infection. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 718–726.     

Stress‐induced changes in color expression mediated by iridophores in a polymorphic lizard

Stress is an important potential factor mediating a broad range of cellular pathways, including those involved in condition‐dependent (i.e., honest) color signal expression. However, the cellular mechanisms underlying the relationship between stress and color expression are largely unknown. We artificially elevated circulating corticosterone levels in male tawny dragon lizards, Ctenophorus decresii, to assess the effect of stress on the throat color signal. Corticosterone treatment increased luminance (paler throat coloration) and decreased the proportion of gray, thereby influencing the gray reticulations that produce unique patterning. The magnitude of change in luminance for corticosterone‐treated individuals in our study was around 6 “just noticeable differences” to the tawny dragon visual system, suggesting that lizards are likely to be able to perceive the measured variation. Transmission electron microscopy (TEM) of iridophore cells indicated that luminance increased with increasing density of iridophore cells and increased spacing (and/or reduced size) of crystalline guanine platelets within them. Crystal spacing within iridophores also differed between skin colors, being greater in cream than either gray or yellow skin and greater in orange than yellow skin. Our results demonstrate that stress detectably impacts signal expression (luminance and patterning), which may provide information on individual condition. This effect is likely to be mediated, at least in part, by structural coloration produced by iridophore cells.     

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.     

BADGE SIZE,PHENOTYPIC QUALITY,AND REPRODUCTIVE SUCCESS IN THE HOUSE SPARROW: A STUDY ON HONEST ADVERTISEMENT

Honest signaling theory suggests that advertising traits must be costly to their bearer; thus, only individuals of high phenotypic quality can exhibit maximal expression of these traits. Males of the sexually dichromatic house sparrow, Passer domesticus, have a black throat patch that functions as a badge of status. I investigated whether badge size honestly shows phenotypic quality. Badge size increases with age and decreases with advancing fledging date in yearling males; thus, badge size was larger in older individuals even though age differences were small. Badge size also increased with physical condition independent of age. These results indicate that badge size functions as an honest signal, possibly because there are costs involved in its production. I also found that males with enlarged badges acquired more nest sites than either control males or males with reduced badges. However, males with enlarged badges possessing a nest site raised fewer fledglings per year than did males with reduced badges, suggesting that cheating has no selective benefit. Further studies that accurately measure the energy expenditure allocated to badge production and that quantify additional fitness components are needed to clarify how reliable badges are maintained.     

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’.     

Parental Feeding Rates in the House Sparrow,Passer domesticus: Are Larger‐Badged Males Better Fathers?

Elaborated secondary sexual characteristics may reflect genetic quality or good health, either of which may be associated with an individual's competence as a parent. We examined whether female house sparrows (Passer domesticus) paired to large vs. small‐badged mates gain benefits in the form of increased parental care or improved nestling welfare. House sparrow nests where the male had been trapped and banded were observed for 1 h on at least 5 d during the peak growth period of nestlings. Male feeding shares, measured as the proportion of total feeds per chick made by the male, were marginally positively correlated with male badge size. Moreover, higher male shares of nestling feeding were associated with improved prospects for offspring survival, and a greater proportion of chicks fledged from the nests of larger‐badged males. These results suggest that females paired to large‐badged males gain direct benefits in the form of enhanced nestling survival, which presumably stem from factors associated with increases in the proportion of nestling feeding contributed by their mates.     

Changes in expression and honesty of sexual signalling over the reproductive lifetime of sticklebacks

Fitness costs of signalling are essential in order for reliable sexual signalling to prevail when the interests of the sexes conflict. This means that signalling can be subjected to a life history trade-off between present and future signalling effort. Here, I show that three-spined stickleback males (Gasterosteus aculeatus), who have a single breeding season during which they breed repeatedly, change their red nuptial coloration over the season depending on their body size at the start of breeding. Large males that completed several breeding cycles increased their red coloration over the season, whereas small males, who completed only a few cycles, did not. The increase in coloration was accompanied by an increase in parental success when males were energy constrained, but not when they had access to an unlimited food supply. Red coloration was thus an honest signal of male parental ability despite changes in signal expression when both signalling and parental care were costly and the investments in them changed simultaneously over the reproductive lifetime. However, the honesty of the signal varied over a lifetime. At the penultimate cycle, bright males cannibalized some of their eggs, probably to increase survival to the last cycle, whereas males cared for their offspring independent of coloration at the ultimate cycle.     

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.     

Beyond illness: Variation in haemosporidian load explains differences in vocal performance in a songbird

In animal communication, signals are expected to evolve to be honest, so that receivers avoid being manipulated by signalers. One way that signals can evolve to be honest is for them to be costly, with only high‐quality individuals being able to bear the costs of signal expression. It has been proposed that parasites can introduce costs that affect the expression of sexually selected traits, and there is evidence to support the role of parasitism in modulating animal behavior. If host infection status or intensity is found to relate to differences in signal expression, it may indicate a fitness cost that mediates honesty of signals. Birdsong is a good model for testing this, and physically challenging songs representing complex motor patterns provide a good example of sexually selected traits indicating individual condition. We performed a field study to evaluate the relationship between song performance and avian malaria infection in a common songbird. Previous work on this subject has almost always evaluated avian malaria in terms of binary infection status; however, parasitemia—infection intensity—is rarely assessed, even though differences in parasite load may have profound physiological consequences. We estimated parasitemia levels by using real‐time PCR. We found that birds with higher parasitemia displayed lower vocal performance, providing evidence that this song trait is an honest signal of parasitic load of haemosporidian parasites. To our knowledge, this study links parasite load and the expression of a sexually selected trait in a way that has not been addressed in the past. Studies using song performance traits and parasitemia offer an important perspective for understanding evolution of characters via sexual selection.     

Protein pheromone expression levels predict and respond to the formation of social dominance networks

Communication signals are key regulators of social networks and are thought to be under selective pressure to honestly reflect social status, including dominance status. The odours of dominants and nondominants differentially influence behaviour, and identification of the specific pheromones associated with, and predictive of, dominance status is essential for understanding the mechanisms of network formation and maintenance. In mice, major urinary proteins (MUPs) are excreted in extraordinary large quantities and expression level has been hypothesized to provide an honest signal of dominance status. Here, we evaluate whether MUPs are associated with dominance in wild‐derived mice by analysing expression levels before, during and after competition for reproductive resources over 3 days. During competition, dominant males have 24% greater urinary MUP expression than nondominants. The MUP darcin, a pheromone that stimulates female attraction, is predictive of dominance status: dominant males have higher darcin expression before competition. Dominants also have a higher ratio of darcin to other MUPs before and during competition. These differences appear transient, because there are no differences in MUPs or darcin after competition. We also find MUP expression is affected by sire dominance status: socially naive sons of dominant males have lower MUP expression, but this apparent repression is released during competition. A requisite condition for the evolution of communication signals is honesty, and we provide novel insight into pheromones and social networks by showing that MUP and darcin expression is a reliable signal of dominance status, a primary determinant of male fitness in many species.     

The crest of the peafowl: a sexually dimorphic plumage ornament signals condition in both males and females

Both male and female peafowl grow crests on top of their head – iridescent blue in males, dull iridescent green and brown in females – but the potential signal function of this plumage ornament is unknown. In this study, peafowl crests were measured in three feral populations, and morphological variation in this ornament was studied in relation to body condition (body mass in relation to tarsus length) and health (white blood cell concentration and ectoparasite load). Prior to the start of the breeding season, male crests are wider with greater pennaceous area, and are more likely to have all feathers grown out compared with female crests. Only crest length changed with measurement date, increasing over time; in males, crest measurements were not related to the extent of train feather development. Crest morphology is a potential signal of individual health and condition in both sexes, but in different ways. In females, the amount of crest plumage grown out to its full extent was related to body condition at the start of the breeding season, whereas in males, the size and pennaceous area of the ornament were related to ectoparasite load. Observations of within‐sex agonistic behaviour suggest a possible role for the crest ornament in status signaling in males, because males that engage in more aggressive interactions tend to have wider crests. There was no evidence for a relation between crest morphology and agonistic behaviour in females.     

Differential selection according to the degree of cheating in a status signal

The maintenance of honesty in a badge-of-status system is not fully understood, despite numerous empirical and theoretical studies. Our experiment examined the relationship between a status signal and winter survival, and the long-term costs of cheating, by manipulating badge size in male house sparrows, Passer domesticus. The effect of badge-size manipulation on survival was complex owing to the significant interactions between the treatments and original (natural) badge size, and between the treatments and age classes (yearlings and older birds). Nevertheless, in the experimental (badge-enlargement) group, males with originally large badges had increased winter survival, while males with originally small badges had decreased survival. This indicates that differential selection can act on a trait according to the degree of cheating.     

Carotenoid‐based plumage colouration is predicted by age and parasites in the male European serin

A fundamental assumption of theories on the evolution of sexual signals is that they should be costly to produce in order to honestly signal the quality of the sender. The expression of carotenoid‐based plumage signals is considered to be condition‐dependent, due to the role of carotenoids functioning as pigments and as health modulators. We assessed carotenoid‐based plumage colouration in relation to male condition in a free living population of male European serins Serinus serinus during the breeding season. Male serins were trapped for morphometric and colouration measurements, during a four‐year field study, in order to evaluate the signalling value of colouration in relation to body condition and parasites level. We compared two different forms of colour quantification based on spectral data – the most commonly used tristimulus colour variables and physiological models of avian colour vision – and found that they were highly correlated for this species. We investigated the signalling value of male plumage colouration and it was found to be related to age and ectoparasite load. Plumage double cone and patch size were negatively related to parasites level, whereas SWS ratio was positively related to parasites and age. Colouration was also related with the time since moult. Our results indicate that the colour expression of serin's plumage is age dependent and is related, in complex ways, with the ability to cope with parasitic infection.