Honest Signal Of Individual Quality Research Articles

Captivity affects mitochondrial aerobic respiration and carotenoid metabolism in the house finch (Haemorhous mexicanus).

In many species of animals, red carotenoid-based coloration is produced by metabolizing yellow dietary pigments, and this red ornamentation can be an honest signal of individual quality. However, the physiological basis for associations between organism function and the metabolism of red ornamental carotenoids from yellow dietary carotenoids remains uncertain. A recent hypothesis posits that carotenoid metabolism depends on mitochondrial performance, with diminished red coloration resulting from altered mitochondrial aerobic respiration. To test for an association between mitochondrial respiration and red carotenoids, we held wild-caught, molting male house finches in either small bird cages or large flight cages to create environmental challenges during the period when red ornamental coloration is produced. We predicted that small cages would present a less favorable environment than large flight cages and that captivity itself would decrease both mitochondrial performance and the abundance of red carotenoids compared with free-living birds. We found that captive-held birds circulated fewer red carotenoids, showed increased mitochondrial respiratory rates, and had lower complex II respiratory control ratios - a metric associated with mitochondrial efficiency - compared with free-living birds, though we did not detect a difference in the effects of small cages versus large cages. Among captive individuals, the birds that circulated the highest concentrations of red carotenoids had the highest mitochondrial respiratory control ratio for complex II substrate. These data support the hypothesis that the metabolism of red carotenoid pigments is linked to mitochondrial aerobic respiration in the house finch, but the mechanisms for this association remain to be established.

Male aggressiveness during the female fertile phase in relation to extra-pair paternity, plumage ornaments and female traits

In many bird species, physical aggression between males become more frequent during the female’s fertile period, as female encounters with extra-pair males are more frequent and can entail paternity losses. Male aggressiveness during this stage has been proposed as crucial for ensuring male reproductive success. Thus, plumage ornaments could represent honest signals of individual quality that could reflect the aggressiveness of paired territorial males. Furthermore, male aggressiveness could be related to mate quality or defensive capacity. We quantified extra-pair paternity in the broods and investigated the association of male and female traits with the aggressive behaviour of territorial paired males in a Spanish population of Pied Flycatchers (Ficedula hypoleuca), where territorial intrusions were simulated during the female fertile period by placing a taxidermic male mount close to the nest. We predicted that (1) more aggressive males should better protect their mates from intruding males and thereby reduce their paternity losses, (2) males with larger white patches and higher UV reflectance of wing patches should respond more strongly to intrusions, and (3) that males should be more aggressive when mated with higher quality females. We found evidence that males that responded less intensely to a territorial intrusion suffered a higher paternity loss, which offers strong support to the basic tenet of the theory of territoriality as paternity defence. Moreover, both the level of male aggressiveness and control of the territory increased with male UV reflectance of wing patches. Finally, we found, contrary to our prediction, that males were less aggressive when mated with more ornamented females.

Development and genetics of red coloration in the zebrafish relative Danio albolineatus.

Animal pigment patterns play important roles in behavior and, in many species, red coloration serves as an honest signal of individual quality in mate choice. Among Danio fishes, some species develop erythrophores, pigment cells that contain red ketocarotenoids, whereas other species, like zebrafish (D. rerio) only have yellow xanthophores. Here, we use pearl danio (D. albolineatus) to assess the developmental origin of erythrophores and their mechanisms of differentiation. We show that erythrophores in the fin of D. albolineatus share a common progenitor with xanthophores and maintain plasticity in cell fate even after differentiation. We further identify the predominant ketocarotenoids that confer red coloration to erythrophores and use reverse genetics to pinpoint genes required for the differentiation and maintenance of these cells. Our analyses are a first step toward defining the mechanisms underlying the development of erythrophore-mediated red coloration in Danio and reveal striking parallels with the mechanism of red coloration in birds.

Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird.

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black - the breeding colours - and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19-0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.

Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

Sexually selected traits are hypothesized to be honest signals of individual quality due to the costs associated with their maintenance, development, and/or production. Testosterone, a sex steroid associated with the development and/or production of sexually selected traits, has been proposed to enforce the honesty of sexually selected traits via its immunosuppressive effects (i.e., the Immunocompetence Handicap Hypothesis) and/or by influencing an individual’s exposure/susceptibility to oxidative stress (i.e., the Oxidation Handicap Hypothesis). Previous work testing these hypotheses has primarily focused on physiological measurements of immunity or oxidative stress, but little is known about the molecular pathways by which testosterone could influence immunity and/or oxidative stress pathways. To further understand the transcriptomic consequences of experimentally elevated testosterone in the context of handicap hypotheses, we used previously published RNA-seq data from studies that measured the transcriptome of individuals treated with either a testosterone-filled or an empty (i.e., control) implant. Two studies encompassing three species of bird and three tissue types fit our selection criteria and we reanalyzed the data using weighted gene co-expression network analysis. Testosterone-treated individuals exhibited signatures of immunosuppression and our results describe the molecular pathways underlying this effect. We also provide some evidence to suggest that the transcriptomic signature of immunosuppression is evolutionarily conserved between the three species. While our results provide no evidence to suggest testosterone mediates handicaps via pathways associated with oxidative stress, they do support the hypothesis that testosterone enforces the honesty of sexually-selected traits by influencing an individual’s immunocompetence. Overall, this study develops a framework for testing testosterone-mediated handicap hypotheses and provides guidelines for future integrative and comparative studies focused on the proximate mechanisms mediating sexually selected traits.

An experimental test of mate choice for red carotenoid coloration in the marine copepod Tigriopus californicus

AbstractColorful ornaments are hypothesized to have evolved in response to sexual selection for honest signals of individual quality that provide information about potential mates. Red carotenoid coloration is common in diverse groups, and in some vertebrate taxa, red coloration is a sexually selected trait whereby mates with the reddest ornaments are preferred. Despite being widespread among invertebrates, whether red carotenoid coloration is assessed during mate choice in these taxa is unclear. The marine copepod Tigriopus californicus displays red coloration from the accumulation of the carotenoid astaxanthin. Previous research on copepods has shown that astaxanthin provides protection from UV radiation and xenobiotic exposure and that carotenoid production is sensitive to external stressors. Because of the condition dependency of the red coloration, we hypothesized that Tigriopus would use it as a criterion during mate choice. To test this hypothesis, we conducted trials in which males chose between females that were wild‐type red (carotenoid‐rich algae diet) or white (carotenoid‐deficient yeast diet). To control for dietary differences and to isolate the effect of carotenoid coloration, we also presented males with restored‐red females fed a carotenoid‐supplemented yeast diet. We found that wild‐type red females were weakly preferred over white females. After controlling for diet, however, we found that restored‐red females were avoided. Our observations do not support the hypothesis that male copepods prefer the carotenoid coloration of females during mate choice. We hypothesize that algal‐derived compounds other than carotenoids play a role in mate choice. Red coloration in copepods appears to be a condition‐dependent trait that is not assessed during mating.

Mite load predicts the quality of sexual color and locomotor performance in a sexually dichromatic lizard.

Since Darwin, the maintenance of bright sexual colors has recurrently been linked to mate preference. However, the mechanisms underpinning such preferences for bright colors would not be resolved for another century. Likely, the idea of selection for colors that could decrease the chances of survival (e.g., flashy colors that can inadvertently attract predators) was perceived as counterintuitive. It is now widely accepted that these extreme colors often communicate to mates the ability to survive despite a “handicap” and act as honest signals of individual quality when they are correlated with the quality of other traits that are directly linked to individual fitness. Sexual colors in males are frequently perceived as indicators of infection resistance, in particular. Still, there remains considerable discord among studies attempting to parse the relationships between the variables associating sexual color and infection resistance, such as habitat type and body size. This discord may arise from complex interactions between these variables. Here, we ask if sexual color in male Florida scrub lizards (Sceloporus woodi) is an honest signal of resistance to chigger mite infection. To this end, we use linear modeling to explore relationships between mite load, different components of sexual color, ecological performance, body size, and habitat type. Our data show that that the brightness of sexual color in scrub lizards is negatively associated with the interaction between mite load and body size, and scrub lizards suffer decreased endurance capacity with increases in mite load. Our data also indicate that mite load, performance, and sexual color in male scrub lizards can vary between habitat types. Collectively, these results suggest that sexual color in scrub lizards is an honest indicator of individual quality and further underscore the importance of considering multiple factors when testing hypotheses related to the maintenance of sexual color.

Male Red-crested Cardinal plumage coloration is associated with parental abilities and breeding performance

Avian plumage coloration deriving from carotenoid-based pigments is among the most honest signals of individual quality. It has been argued that females may differentially allocate resources based on mate attractiveness or quality, paying the costs of investing more in a current breeding attempt. We tested predictions of the differential allocation hypothesis on the natural variation of carotenoid-based plumage using the brightly red-colored head plumage of the Red-crested Cardinal (Paroaria coronata). It is to our knowledge the first time this hypothesis is tested on the natural variation of this pigment on a wild bird. We found that the brightness of the males’ red plumage patch is positively associated with their reproductive success and the nest defence they provide. We also found that brighter males invest less in their offspring (by delivering less food to their nestlings and poorly cleaning the nest) than duller males and, by contrast, females mated with brighter males invest more in parental care. Our results are consistent with the differential allocation hypothesis: differential allocation allowed breeding pairs with brighter males to produce more offspring, suggesting that it can be considered adaptive and should be included in studies of eco-evolutionary dynamics.

Melanin-based plumage ornamentation signals condition and physiological stress in the Black-headed Gull

There is increasing evidence that melanin-based plumage ornaments play a role in the sexual selection of birds, although there seems to be little consensus on the mechanisms underlying the signalling function of melanin-based plumage. The aim of this study was to assess the potential of a melanin-based plumage ornament (brown hood) to reflect components of individual quality (condition and physiological stress) in a common larid species, the Black-headed Gull Chroicocephalus ridibundus. For this purpose, we measured the size of the hood in over 500 Black-headed Gulls captured in several breeding colonies distributed across Poland. We found that hood size correlated positively with blood haemoglobin concentration, although we found no evidence for a relationship with blood glucose concentration or body mass. There was also a negative relationship between hood size and physiological stress, as assessed by leucocyte profiles (heterophil/lymphocyte ratio). We found this correlation in both sexes, suggesting that hood size may be an honest signal of individual quality in males and females, which implies a mutual mate choice in the Black-headed Gull. Finally, the relationship between hood size and blood haemoglobin concentration was primarily attributed to the parallel variation of these traits among the colonies, suggesting that Black-headed Gulls may settle in colonies in a despotic manner. As far as we are aware, our study is one of the first to show an honest signalling role of melanin-based ornaments in the gull family, Laridae. It remains to be tested whether different melanin-based plumage ornaments in gulls are developmentally and functionally integrated with each other and with carotenoid-based integument coloration.

Males with More Pheomelanin Have a Lower Oxidative Balance in Asian Barn Swallows (Hirundo rustica gutturalis).

Pheomelanin-based plumage pigmentation has been suggested to be an honest signal of individual quality to conspecifics. It has been hypothesized that oxidative stress is an important agent linking pheomelanic pigmentation to individual quality. Using the Asian barn swallow Hirundo rustica gutturalis, a wild passerine, we tested whether the pheomelanin pigmentation in the red throat patch of adult males, a sexually selected trait, is associated with the ratio between reduced and oxidized glutathione (RGSH/GSSG) as an indicator of current oxidative balance during the early breeding season. We found that males with a higher pheomelanin concentration in their throat feathers had a significantly lower RGSH/GSSG ratio (i.e., higher oxidative stress), but exhibited a better body condition, measured as residual body mass on body size, compared to males with a lower pheomelanin concentration. The total GSH level was not significantly related to the pheomelanin concentration. These findings suggest a negative association between the red pheomelanin pigmentation and oxidative balance during mating and reproductive efforts, which might be mitigated by high-quality males. Further research is needed to understand its actual damage and mitigation mechanism.

Carotenoid metabolism strengthens the link between feather coloration and individual quality

Thirty years of research has made carotenoid coloration a textbook example of an honest signal of individual quality, but tests of this idea are surprisingly inconsistent. Here, to investigate sources of this heterogeneity, we perform meta-analyses of published studies on the relationship between carotenoid-based feather coloration and measures of individual quality. To create color displays, animals use either carotenoids unchanged from dietary components or carotenoids that they biochemically convert before deposition. We hypothesize that converted carotenoids better reflect individual quality because of the physiological links between cellular function and carotenoid metabolism. We show that feather coloration is an honest signal of some, but not all, measures of quality. Where these relationships exist, we show that converted, but not dietary, carotenoid coloration drives the relationship. Our results have broad implications for understanding the evolutionary role of carotenoid coloration and the physiological mechanisms that maintain signal honesty of animal ornamental traits.

Variation in melanin pigmentation of a sexually selected plumage trait and its adaptive value in the Common Snipe Gallinago gallinago

There is increasing evidence that melanin‐based plumage coloration correlates with different components of fitness and that it may act as a social or sexual signal of individual quality. We analysed variation in melanin pigmentation in the outermost tail feathers of the Common Snipe Gallinago gallinago. During courtship flights, male Snipe use their outermost tail feathers to generate a drumming sound, which plays a role in territory establishment and mate choice. As the outermost tail feathers are displayed to females during these flights, we predicted that conspicuous variation in their rusty‐brown (pheomelanin‐based) coloration may act as an honest signal of individual quality. To test this prediction, we spectrophotometrically measured brightness (an indicator of total melanin content) and red chroma (an indicator of pheomelanin content) of the outermost tail feathers in 180 juvenile and adult Common Snipe. An age‐related decline in feather brightness was found exclusively in females, suggesting that melanization could have evolved by natural selection to camouflage incubating birds. In both sexes, brightness of the tail feathers was inversely correlated with their structural quality (as measured with mass–length residuals), suggesting that melanization could increase mechanical properties of feathers and, in males, enhance the quality of courtship sonation. Red chroma positively correlated with total plasma protein concentration, supporting our prediction that pheomelanin pigmentation of tail feathers may act as an honest signal of condition. Our study indicated that variation in the melanin‐based coloration of the outermost tail feathers in the Common Snipe could have evolved as a result of several different selection pressures and it emphasizes the complexity of the processes that underlie the evolution of melanin‐based plumage coloration in birds.

Sexual display complexity varies non-linearly with age and predicts breeding status in greater flamingos.

The long-lived greater flamingo (Phoenicopterus roseus) is famous for performing conspicuous group displays during which adults try to acquire a new mate each year with varying success. We examined variation in the sexual display complexity (SDC) of wild flamingos aged between 4 and 37 yrs. SDC was defined as the product of richness (the number of different display movements) and versatility (the number of transitions between movements) within a 5 min behavioral sequence. In both sexes, date in the pairing season had a linear and positive effect on SDC, whereas age had a quadratic effect, with SDC increasing until about age 20yrs, and declining afterwards. SDC better explained pairing patterns than age, and positively influenced the probability of becoming a breeder. Our results thus support the idea that SDC is an honest signal of individual quality and further suggest that senescence in display could be an overlooked aspect of reproductive decline in species with no or weak pair bonding.

Testosterone levels in relation to size and UV reflectance of achromatic plumage traits of female pied flycatchers

In a substantial number of species, females show some development of secondary sexual characters. These traits can function as signals of individual phenotypic or genetic qualities and status to conspecifics. Individuals may benefit potentially from expressing signals or badges of status if they are reliable and honest signals of individual quality. In many species, badge sizes have been shown to correlate with dominance rank, which may be mediated by testosterone (T) levels. Here, we explored geographic variation in the size and properties of the white wing patch of female pied flycatchers Ficedula hypoleuca and its relation to circulating T levels in three populations (two southern populations in central Spain and a northern population in Finland). Furthermore, we aimed at detecting if the size of the white wing patch and its ultraviolet (UV) reflectance indicate individual quality. We found that females in Spain had larger, brighter and more UV reflecting wing patches than those in Finland. Females with higher UV reflectance and larger primary white patches bred earlier. Younger females and females with larger primary white wing patches showed higher T levels. In contrast, higher values of UV reflectance in feathers from these patches were associated with low T levels. Despite genetic differentiation and differences in trait expression between populations, female pied flycatchers from different populations may converge and use the size of white wing patches to signal their T levels and thereby their social dominance.

Nestling sex and plumage color predict food allocation by barn swallow parents

Despite parents are equally related to all of their progeny, they may differentially invest in offspring that provide the highest fitness return. Sons and daughters can differ in reproductive value, especially in species where fitness is predicted by the expression of sexually selected traits. In many birds, offspring plumage coloration functions as a honest signal of individual quality, thus allowing parents to differentially invest in offspring of either sex accordingly. Here, we tested whether parents allocate different amounts of food depending on plumage color of their male and female offspring. As a model, we used the barn swallow (Hirundo rustica), a species where large among- and within-brood variation in ventral plumage color exists and male reproductive success varies according to ventral plumage coloration. We recorded the proportion of feedings obtained and body mass variation by dyads of same-sex and similar-sized nestlings subjected to either experimental darkening of their ventral plumage color or to a sham treatment. Plumage darkening enhanced food provisioning and body mass gain of males but not of females. Because darker ventral coloration is associated with larger reproductive success in male barn swallows, these results suggest that parents tune their effort toward more valuable male offspring that are likely to provide the greatest fitness returns. Our study thus suggests that parents are selected to differentially invest in offspring of either sex according to a trait expressed in early life, which is relevant to intrasexual competition for access to mates at sexual maturity.

Causes and consequences of individual variation in the extent of post-juvenile moult in the blue titCyanistes caeruleus(Passeriformes: Paridae)

Moult, comprising the growth or replacement of feathers in birds, is an energetically demanding process. As a result, in many species, the extent of the post-juvenile moult can vary substantially. However, the reasons underlying this variation remain poorly understood, and the potential life-history consequences of variation in moult extent are even less clear. In the present study, we aimed to use individual-specific data to identify factors affecting the extent of the post-juvenile moult in a population of over 2500 blue tits Cyanistes caeruleus Linnaeus 1758, and to assess the consequences of individual variation in moult extent on reproduction in the first year of life. There was a substantial sex difference in post-juvenile moult extent, with males moulting more extensively than females. Putative immigrant birds had moulted on average less than those born locally. However, there was little evidence of carry-over effects of the natal environment on moult extent because we found no relationship between moult extent and fledging date or nestling mass. Evidence that moult extent, and hence feather brightness, affected subsequent reproductive success was limited. Moult extent had no effect on recruitment in males, although female recruits had moulted significantly less than nonbreeders. Because it was not influenced by features of the natal environment, moult extent may not be an honest signal of individual quality in C. caeruleus. As a result, the potential consequences of variation in moult extent for fitness are likely to be small.

Multiple colour traits signal performance and immune response in the Dickerson’s collared lizard Crotaphytus dickersonae

Conspicuous male coloration is often an honest signal of individual quality. In Dickerson’s collared lizard (Crotaphytus dickersonae), males are striking blue, have a black and white collar and have white spots on their bodies. In this study, we investigated whether this extravagant colour pattern is an indicator of male performance in variables related to resource-holding power (bite force, running speed and endurance) and immune condition (cellular response and ectoparasite load). Also, we assessed direct and indirect effects of testosterone levels and body temperature on colour traits. We found that males with bluer skin, and darker and bigger black collars performed better in variables related to resource-holding power. Also, the black colour of the collar was related to immune condition. Blue chroma was positively related to temperature, yet males with bigger and darker black collars had lower body temperatures. Testosterone had minor effects on immune response and colour traits. Our results suggest that multiple colour traits in the Dickerson’s collared lizard may honestly indicate physical and physiological performance.

Relationships between plumage coloration, diet diversity, and winter body condition in the Lesser Goldfinch

Bright and colorful plumage is thought to be an honest signal of individual quality in birds because consuming high-quality forage results in more colorful plumage. To gain insight into the ecological and evolutionary context of the relationship between color, body condition, and diet, we studied a mostly urban population of Lesser Goldfinches (Spinus psaltria). We collected body measurements and digital photographs of plumage, as well as feathers and blood of goldfinches during three winters (2009–2012) in northern Nevada, USA. We analyzed the body tissues (feathers and blood) for stable isotope values of carbon and nitrogen to infer the diets of individual goldfinches, and quantified CIELAB color space values of chroma, brightness, and hue of plumage from the digital images. We then examined the relationships between color values and body condition, and color and stable isotope values. We found that the brightness (L* value) of the back plumage was correlated with both body condition and with stable isotope values of nitrogen (δ15N) in the winter diet. Furthermore, stable isotope analyses of both feathers and blood showed temporal differences in diet. However, hue and chroma, which are color values that are thought to more directly represent feather carotenoid content, were not related to body condition or diet. Our results suggest that the foraging ecology of Lesser Goldfinches changes over time, and that, in winter, plumage color values that are putatively indicative of carotenoid content do not seem to be an honest signal of individual quality as measured by body condition.

A test of the effect of testosterone on a sexually selected carotenoid trait in a cardueline finch

AbstractA great number of secondary sexual traits are assumed to have evolved as honest signals of individual quality. It is known that androgens regulate many male secondary traits as well as reproductive behavior. The expression of melanin‐based coloration is modulated by androgens, particularly testosterone, and there is some evidence that carotenoid‐based coloration may also be under androgen control. In the European serin, Serinus serinus, male carotenoid‐based plumage coloration is a sexually selected trait, subjected to female choice. In this experiment, we investigated if testosterone influences the expression of this trait by manipulating testosterone levels during molt and assessing how it affected plumage color expression after molt. We found that testosterone had only a negative effect on the size of the yellow ornament. Our experiment shows that testosterone had a limited effect on carotenoid‐based coloration of a cardueline finch.

Is carotenoid ornamentation linked to the inner mitochondria membrane potential? A hypothesis for the maintenance of signal honesty

Several mechanistic hypotheses have been proposed for how carotenoid pigmentation of integumentary structures can serve as an honest signal of individual quality. These hypotheses are founded on proposed links between carotenoids, immuno responsiveness, and oxidative stress, but an absence of biochemical information on the oxidative pathways of carotenoids has limited the sophistication of such hypotheses. Based on published evidence, we propose that the oxidation of carotenoids for the purpose of ornamentation in birds and reptiles is coupled to the inner mitochondria membrane. We predict that several carotenoid oxidation reactions yielding ornamental pigments occur on the inner mitochondrial membrane. Three of these reactions are proposed to occur within the ubiquinone biosynthesis cluster known as the Coq cluster consisting of approximately a dozen Coq members, tightly integrated and intimately associated with Complex I and III of the electron transport system. Ubiquinone and highly oxidized ornamental carotenoids share a stereochemically-conserved binding region suggesting that these two molecules may have shared similar pathways in the past. Carotenoids and ubiquinones may cooperate as redox participants in anti-radical reactions or independently in helping to maintain membrane or supra-complex stabilization during times of high-energy demand. Under this hypothesis, oxidation of carotenoids is coupled to the inner mitochondria membrane potential such that ornamental coloration reflects the efficiency of cellular respiration.