Red Ornaments Research Articles

Hidden in red: evidence for and against red camouflage in a jumping spider (Saitis barbipes)

Investigating the conspicuousness of animal color patterns to different observers is crucial for understanding their function. This study examines the peculiar case of a jumping spider (Saitis barbipes) whose males display red and black ornaments during courtship despite an apparent inability to distinguish these colors. We propose that, through predator eyes, red may actually be a better match than black to the spiders’ leaf litter background, and that the black fringe of hairs surrounding red ornaments may blur with red at natural predator acuities and viewing distances to produce a background-matching desaturated red. In a field experiment, we test whether red ornaments reduce predation relative to red ornaments painted black, and find that, unexpectedly, spiders with red ornaments are more heavily predated upon. Having established birds as the spiders’ primary predators, we image the spiders in their natural habitat using an avian-vision camera. We find their red coloration to have similar color contrast, but lower achromatic contrast, with the background than black coloration. We also find that red and black elements blur together at typical avian acuities and viewing distances to produce lower chromatic and achromatic contrasts with the background than would be seen by animals with higher acuities and/or closer viewing distances. Interestingly, red ornaments appear orange or yellow when viewed obliquely, which reduces their achromatic, but not chromatic, contrast with the background. Our imaging results provide support for our hypothesis that red is camouflaging, whereas the results of our predation experiment do not. Any functional significance of the spiders’ red coloration therefore remains unresolved.

Early Oxidative Stress May Prevent a Red Ornament From Signaling Longevity.

Harsh early environmental conditions can exert delayed, long-lasting effects on phenotypes, including reproductive traits such as sexual signals. Indeed, adverse early conditions can accelerate development, increasing oxidative stress that may, in turn, impact adult sexual signals. Among signals, colorations produced by red ketocarotenoids seem to depend on mitochondrial functioning. Hence, they could reveal individual cell respiration efficiency. It has been hypothesized that these traits are unfalsifiable "index" signals of condition due to their deep connection to individual metabolism. Since mitochondrial dysfunction is frequently linked to aging, red ketocarotenoid-based ornaments could also be good signals of a critical fitness component: longevity. We tested this red color per longevity correlation in captive zebra finches. In addition, we experimentally decreased the synthesis of glutathione (a critical intracellular antioxidant) during the first days of the birds' life to resemble harsh early environmental conditions (e.g., undernutrition). Longevity was recorded until the death of the last bird (almost 9 years). Males, but not females, exhibiting a redder bill in early adulthood lived longer than males with paler bills, which agrees with some precedent studies. However, such bill redness-longevity connection was absent among males with inhibited glutathione synthesis. These findings may suggest that environmental factors can alter the reliability of red ketocarotenoid-based sexual signals, making them less unfalsifiable than believed.

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.

Testosterone Coordinates Gene Expression Across Different Tissues to Produce Carotenoid-Based Red Ornamentation.

Carotenoid pigments underlie most of the red, orange, and yellow visual signals used in mate choice in vertebrates. However, many of the underlying processes surrounding the production of carotenoid-based traits remain unclear due to the complex nature of carotenoid uptake, metabolism, and deposition across tissues. Here, we leverage the ability to experimentally induce the production of a carotenoid-based red plumage patch in the red-backed fairywren (Malurus melanocephalus), a songbird in which red plumage is an important male sexual signal. We experimentally elevated testosterone in unornamented males lacking red plumage to induce the production of ornamentation and compared gene expression in both the liver and feather follicles between unornamented control males, testosterone-implanted males, and naturally ornamented males. We show that testosterone upregulates the expression of CYP2J19, a gene known to be involved in ketocarotenoid metabolism, and a putative carotenoid processing gene (ELOVL6) in the liver, and also regulates the expression of putative carotenoid transporter genes in red feather follicles on the back, including ABCG1. In black feathers, carotenoid-related genes are downregulated and melanin genes upregulated, but we find that carotenoids are still present in the feathers. This may be due to the activity of the carotenoid-cleaving enzyme BCO2 in black feathers. Our study provides a first working model of a pathway for carotenoid-based trait production in free-living birds, implicates testosterone as a key regulator of carotenoid-associated gene expression, and suggests hormones may coordinate the many processes that underlie the production of these traits across multiple tissues.

An age-related decline in the expression of a red carotenoid-based ornament in wild birds.

The past decades have provided valuable information on how animals age in the wild. However, examples of male reproductive senescence are scarce. In particular, few studies have described an age-related decline in the expression of conspicuous traits influencing mating success. Red ornaments could be good candidates to detect this decline because their expression may depend on the availability of pigments (carotenoids) related to oxidative stress, the latter frequently linked to senescence. Furthermore, it has been argued that efficient mitochondrial metabolism is key to express red carotenoid-based ornaments, and mitochondrial dysfunction is usually associated with senescence. We studied the age-linked expression of a red carotenoid-based trait: the yellow-to-red plumage coloration of male common crossbills (Loxia curvirostra). This coloration has recently been experimentally related to mitochondrial function. Here, we analyzed longitudinal plumage coloration data obtained throughout 28 years in free-living birds. We detected an initial increase in redness during the first 2 years of life and a subsequent decline. The relationship between color and age was unrelated to within-individual body mass variability. As far as we know, this is the first demonstration of an age-related ketocarotenoid-based color decrease detected by simultaneously testing within- and between-individual variability in wild animals.

Fine-scale variation in lip and cheek colour according to the timing of ovulation in women

Various animal species have evolved a sexual communication system with females displaying and males discriminating information about the timing of ovulation through sexual signals. More research is now investigating the potential ovulatory signalling function of female red skin colour in human and non-human primates. However, to date, it is still challenging to draft satisfying hypotheses about the evolution and function of the female red skin colour, due to methodological discrepancies between human and non-human primate studies. The present study used a within-individual design and objective methods to analyse the relationship between fine-scale variation in cheek and lip colour (luminance and redness) and the estimated day of ovulation in 15 cycling women. I found weak evidence that intra-cycle variation in lip luminance only may be less modulated by inter-individual variation, with lips getting slightly darker around ovulation. However, day to day variation in lip luminance is likely imperceptible, meaning that lip luminance may not act as an ovulatory signal in humans. This study adds to the growing research and discussion on the role and evolution of the female red skin colour of human and non-human primates in the context of sexual signalling and mate attraction. In human and non-human primates, red skin and red ornaments are attractive for both sexes and often associated with mating and fertility. While female red skin colour can be informative about the reproductive status and thus influences mating strategies in some primate species, it is not clear if humans share with non-human primates a colourful trait of ovulation. This study shows a weak relationship between lip luminance only and the timing of ovulation. This study adds to the growing research and discussion on the role and evolution of the female red skin colour of human and non-human primates in the context of sexual signalling and mate attraction.

Dietary canthaxanthin reduces xanthophyll uptake and red coloration in adult red-legged partridges.

Carotenoids give color to conspicuous animal signals that are often the product of sexual selection. Knowledge of the mechanisms involved in carotenoid-based signaling is critical to understanding how these traits evolve. However, these mechanisms remain only partially understood. Carotenoids are usually viewed as scarce dietary antioxidants whose allocation to ornaments may trade off against health. This trade-off would ensure its reliability as a signal of individual quality. In the case of red (keto)carotenoids, the literature suggests that some species may show constraints in their uptake. Canthaxanthin is one of the most common ketocarotenoids in red ornaments of animals. It is often commercially used as a dietary supplement to obtain redder birds (e.g. poultry). We increased the dietary canthaxanthin levels in captive red-legged partridges (Alectoris rufa). This species shows red non-feathered parts mostly pigmented by another common ketocarotenoid: astaxanthin. We studied the impact on the uptake of carotenoids and vitamins and, finally, on coloration. We also tested the potential protective effect of canthaxanthin when exposing birds to a free radical generator (diquat). Canthaxanthin did not apparently protect birds from oxidative stress, but interfered with the absorption of yellow carotenoids (lutein and zeaxanthin). Zeaxanthin is a precursor of astaxanthin in enzymatic pathways, and their levels in tissues and eggs were lower in canthaxanthin-supplied birds. This led to lower astaxanthin levels in ornaments and paler coloration. As far as we know, this is the first report of a carotenoid supplementation decreasing animal coloration. The results have implications for understanding carotenoid-based signaling evolution, but also for improving husbandry/experimental procedures.

Do Female Western Mosquitofish,Gambusia affinis,Prefer Ornaments That Males Lack?

AbstractSome species in the family Poeciliidae are known for extravagant male ornaments and courtship behavior (e.g., guppies), but the majority of poeciliids are characterized by coercive male copulation attempts that seem to circumvent female choice. In some lineages with male ornaments, female sensory bias may have preceded the evolution of corresponding male signals. We examined female preferences for colorful ornaments in Western mosquitofish,Gambusia affinis, in which males lack ornamentation and reproduce primarily through coercive mating attempts. We found that females exhibited a positional affinity for males that were artificially ornamented with blue coloration over males that had been treated with a transparent ornament. Females exhibited the opposite effect for males treated with red ornaments. In contrast, focal females did not exhibit behavioral discrimination between two live stimulus females or two models (silver fishing lures) with blue vs. transparent ornaments. This suggests a sexual context for female discrimination between males based on ornament color and whether an ornament was present. Because tribe Gambusiini is the basal branch of family Poeciliidae, the results of this study are consistent with the hypothesis that female responsiveness to male coloration is the ancestral poeciliid character state.

Genetic Architecture of Conspicuous Red Ornaments in Female Threespine Stickleback.

Explaining the presence of conspicuous female ornaments that take the form of male-typical traits has been a longstanding challenge in evolutionary biology. Such female ornaments have been proposed to evolve via both adaptive and nonadaptive evolutionary processes. Determining the genetic underpinnings of female ornaments is important for elucidating the mechanisms by which such female traits arise and persist in natural populations, but detailed information about their genetic basis is still scarce. In this study, we investigated the genetic architecture of two ornaments, the orange-red throat and pelvic spine, in the threespine stickleback (Gasterosteus aculeatus). Throat coloration is male-specific in ancestral marine populations but has evolved in females in some derived stream populations, whereas sexual dimorphism in pelvic spine coloration is variable among populations. We find that ornaments share a common genetic architecture between the sexes. At least three independent genomic regions contribute to red throat coloration, and harbor candidate genes related to pigment production and pigment cell differentiation. One of these regions is also associated with spine coloration, indicating that both ornaments might be mediated partly via pleiotropic genetic mechanisms.

Accumulation of dietary carotenoids, retinoids and tocopherol in the internal tissues of a bird: a hypothesis for the cost of producing colored ornaments.

Carotenoid-based ornaments may have evolved as a consequence of their costs of production, which would assure the reliability of the traits as signals of individual quality. Different costs due to carotenoid allocation to the signal have been proposed, considering the scarcity of these pigments at the environment (ecological cost) and their physiological properties that would trade against the maintenance of the organism. Carotenoids of many red ornaments (ketocarotenoids) are often the result of biotransformation of those pigments abundant in the diet (usually lutein and zeaxanthin). Some authors have suggested that such a conversion implies a cost relevant for signaling because it requires high levels of antioxidant vitamins in the tissues where biotransformation takes place. We explore this hypothesis in red-legged partridges (Alectoris rufa) by analyzing ketocarotenoids in the ornaments (bare parts) and carotenoids, vitamin A in different forms (free and esterified) and vitamin E in blood, liver and fat. Ketocarotenoids in ornaments (astaxanthin and papilioerythrinone) were not found in internal tissues, suggesting that they were directly transformed in the bare parts. However, ketocarotenoid levels where positively correlated with the levels of their precursors (zeaxanthin and lutein, respectively) in internal tissues. Interestingly, ketocarotenoid levels in bare parts negatively and positively correlated with vitamin A and E in the liver, respectively, the same links only being positive in blood. Moreover, retinyl and zeaxanthin levels in liver were negatively related. We hypothesize that storing substrate carotenoids in the main storage site (the liver) implies a cost in terms of regulating the level of vitamin A.

Ultraviolet and carotenoid-based coloration in the viviparous lizardZootoca vivipara(Squamata: Lacertidae) in relation to age, sex, and morphology

Lizards display structural and pigment-based colorations, and their visual system is sensitive to wavelengths of 300–700 nm. However, few studies in squamate reptiles have quantified interindividual colour variation that includes the structural ultraviolet (UV) component (300–400 nm). In the present study, we investigated variability of a ventral UV/yellow–red ornamentation in the common lizard Zootoca vivipara, including an analysis of spatial distribution, as well as sex and age differences. We also investigated whether the expression of coloration is related to body size and condition. Our analyses revealed two distinct patches: a gular patch with a strong UV reflectance and a belly patch with a dominant yellow–red reflectance. Males displayed a less saturated throat coloration with higher UV chroma and UV hue, and had a redder but duller belly coloration than females. Yearlings had less elaborate ornaments than adults, although they already displayed a yellow–red sexual dichromatism on the belly. UV sexual dichromatism was only apparent in adults as a result of a weaker UV reflectance in females, suggesting potential fitness costs of a bright UV coloration in that sex. Different colour traits were related to body size in both sexes, as well as to body condition in males. We discuss the potential evolutionary scenarios leading to the maintenance of this ornament in common lizards. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110, 128–141.

Women's use of red clothing as a sexual signal in intersexual interaction

Research on several non-human primate species has shown that females use red ornamentation as a sexual signal to attract male conspecifics. In the present research, we conducted two experiments designed to test an analogous use of red clothing by women in an intersexual interaction. In Experiment 1, women expecting to converse with an attractive man were more likely to choose to wear a red (versus green) shirt than women expecting to converse with an unattractive man or a woman of average attractiveness. In Experiment 2, women expecting to converse with an attractive man were more likely to choose to wear a red (versus blue) shirt than women expecting to converse with an attractive woman; red shirt choice was positively correlated with attractiveness and status perceptions in the former, but not the later, case. These findings contribute to both the literature on female sexuality and that on color and behavior.

Dressed for sex: red as a female sexual signal in humans.

BackgroundIn many non-human primate species, a display of red by a female serves as a sexual signal to attract male conspecifics. Red is associated with sex and romance in humans, and women convey their sexual interest to men through a variety of verbal, postural, and behavioral means. In the present research, we investigate whether female red ornamentation in non-human primates has a human analog, whereby women use a behavioral display of red to signal their sexual interest to men.Methodology/Principal FindingsThree studies tested the hypothesis that women use red clothing to communicate sexual interest to men in profile pictures on dating websites. In Study 1, women who imagined being interested in casual sex were more likely to display red (but not other colors) on their anticipated web profile picture. In Study 2, women who indicated interest in casual sex were more likely to prominently display red (but not other colors) on their actual web profile picture. In Study 3, women on a website dedicated to facilitating casual sexual relationships were more likely to prominently exhibit red (but not other colors) than women on a website dedicated to facilitating marital relationships.Conclusions/SignificanceThese results establish a provocative parallel between women and non-human female primates in red signal coloration in the mating game. This research shows, for the first time, a functional use of color in women's sexual self-presentation, and highlights the need to extend research on color beyond physics, physiology, and preference to psychological functioning.

Linking sexual selection and behavioral isolation in a colorful species of stream fish, Etheostoma barrenense

Linking sexual selection and behavioral isolation in a colorful species of stream fish, Etheostoma barrenense

Pteridine, not carotenoid, pigments underlie the female-specific orange ornament of striped plateau lizards (Sceloporus virgatus)

Indicator models of sexual selection suggest that signal honesty is maintained via costs of ornament expression. Carotenoid-based visual signals are a well-studied example, as carotenoids may be environmentally limited and impact signaler health. However, not all bright yellow, orange and red ornaments found in vertebrates are carotenoid-based; pteridine pigments may also produce these colors. We examine the contribution of carotenoid and pteridine pigments to the orange reproductive color of female striped plateau lizards (Sceloporus virgatus). This color ornament reliably indicates female mate quality, yet costs maintaining signal honesty are currently unknown. Dietary carotenoid manipulations did not affect orange color, and orange skin differed from surrounding white skin in drosopterin, not carotenoid, content. Further, orange color positively correlated with drosopterin, not carotenoid, concentration. Drosopterin-based female ornaments avoid the direct trade-offs of using carotenoids for ornament production vs egg production, thus may relax counter-selection against color ornament exaggeration in females. Direct experimentation is needed to determine the actual costs of pteridine-based ornaments. Like carotenoids, pteridines influence important biological processes, including immune and antioxidant function; predation and social costs may also be relevant.

Male red ornamentation is associated with female red sensitivity in sticklebacks.

Sexual selection theory proposes correlated evolutionary changes in mating preferences and secondary sexual characters based on a positive genetic correlation between preference and the preferred trait. Empirical work has provided support for a genetic covariation between female preference and male attractiveness in several taxa. Here, we study parent and offspring visual traits in threespine sticklebacks, Gasterosteus aculeatus. While focusing on the proximate basis of mating preferences, we compare the red breeding coloration of males, which strongly contributes to female choice, with their daughters' red sensitivity measured by optomotor response thresholds. We show that the red color expression of fathers correlates well with their daughters' red sensitivity. Given that a within-population genetic correlation between signal and preference was experimentally confirmed for the red coloration in sticklebacks, our results indicate a proximate mechanism in terms of perceptual sensitivity being involved in the co-evolution of female preferences and male mating signals.

Identification of carotenoid pigments and their fatty acid esters in an avian integument combining HPLC–DAD and LC–MS analyses

Yellow-orange-red ornaments present in the integuments (feathers, bare parts) of birds are often produced by carotenoid pigments and may serve to signal the quality of the bearer. Although carotenoid esterification in tissues is a common phenomenon, most of the work on avian carotenoids has been focused on the identification of free forms or have been done after sample saponification. Here we determined free and esterified carotenoid composition in a bird species with red ornaments: the red-legged partridge ( Alectoris rufa). Carotenoids from leg integument were extracted and processed by TLC to separate three major carotenoid groups (free form, mono- and diesters with fatty acids), whereas saponified extracts gave only free forms of carotenoids. TLC fractions were then analyzed by HPLC–DAD with C18 phase column for a preliminary identification of carotenoid groups. The final characterization of free carotenoids and its esters with fatty acids was performed with direct extracts analyzed by LC–MS and LC–MS/MS with a C30 phase, always with a system coupled to DAD. The main carotenoid ( λ max 478 nm and [M+H] + at m/ z 597.2) was identified as astaxanthin by comparison with standards. A second carotenoid ( λ max between 440 and 480 nm and [M+H] + at m/ z 581.3) was not identified among any of the commercially available carotenoid standards, although it could correspond to pectenolone according to its fragmentation pattern. Both the unidentified carotenoid and astaxanthin formed monoesters with fatty acids, but only astaxanthin was in its diesterified form. Monoesters were mainly formed with palmitic, stearic, oleic and linoleic acids. Complementary analyses of fatty acid composition in partridge integument by GC–MS revealed high amounts of these and other fatty acids, such as myristic, arachidic and docosanoic acids. The combination of HPLC–DAD and LC–MS/MS spectra was especially useful to identify the carotenoids present in the esterified forms and the probable masses of the fatty acids included in them, respectively.

Woman with a Fan: Paul Gauguin's Heavenly Vairaumati—a Parable of Immortality

Woman with a Fan (1902) is the culmination of Gauguin's representations of the Tahitian goddess of regeneration. His depiction of Vairaumati frames his intertwined aesthetic and spiritual beliefs. Her fan signals her immortal status and, through its blue, white, and red ornament, Gauguin's revolutionary call to “the right to dare all.” This justifies his assimilation of multiple sources, which, through a process he called transposition, took on new life. Thus, the regeneration epitomized by Vairaumati is implemented in the pictorial dynamic through the mutation of the sources that constitute her identity, tying the permutations of art to the soul's immortality.

Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross

Orchids are one of the most unique and evolved of flowering plants, with many being valuable floricultural crops. Spatial localization of pigments within the flower of the commercially important bi-color Oncidium Gower Ramsey demonstrated a mixture of carotenoids and anthocyanins concentrated in the adaxial epidermis. Chromatography identified the predominant yellow pigment to be an equal mixture of all-trans and 9-cis isomers of violaxanthin, with esterification specific to the 9-cis isomer. Red ornamentation was comprised of the anthocyanins cyanidin and its methylated derivate, peonidin. Five key pigment biosynthesis genes encoding dihydroflavonol 4-reductase (DFR), phytoene synthase (PSY), phytoene desaturase, carotenoid isomerase, and the downstream 9-cis epoxycarotenoid dioxygenase were isolated and their expression profiles determined. Northern analyses showed both phytoene desaturase and carotenoid isomerase expression to be up-regulated in floral tissue relative to leaves whereas PSY was not. Three closely related DFR genes were isolated, including one with an insertion in the 3' coding region. DFR expression occurred throughout flower development in Oncidium, unlike in Dendrobium and Bromheadia orchids. A number of the isolated anthocyanin and carotenoid genes showed variations due to insertion events. These findings raise questions about the genetic stability in interspecific crosses in orchids, such as the tri-specific Oncidium Gower Ramsey.

Do male sticklebacks prefer females with red ornamentation?

In general, females are less ornamented than males and until recently female ornaments have been regarded as non-adaptive correlated effects of selection on males. This view is challenged and the alternative hypothesis that females' ornaments have evolved independently of male showiness, by intersexual selection for example, is supported. I tested these hypotheses experimentally using threespine sticklebacks (Gasterosteus aculeatus) from a population in which both sexes have red pelvic spines. Two females differing in red spine colour extravagance were presented simultaneously to a male under white and green light, and the male's courtship activity towards each female was quantified. Green light prevented the use of red cues by sticklebacks. The results show that red colour on the pelvic spines of female sticklebacks has value as a signal to males in this population, and males actually courted females with drab pelvic spines more than females whose pelvic spines had a redder hue, but only when illuminated by white light. The interpretation that best accounts for this result is that spine colour has a strong function in male–male aggressive interactions. This interpretation favours the hypothesis of non-adaptive correlation that has been proposed to explain the evolution of red spines in female sticklebacks.