Responses of disparate phenotypically-plastic,melanin-based traits to common cues: limits to the benefits of adaptive plasticity?

The evolution of perfect adaptive phenotypic plasticity of a given trait may be influenced by, among other things, phenotypic costs associated with the expression of a given trait value, relative to alternative trait values. One potential cause of such phenotypic costs is the allocation of limited resources to multiple traits. When multiple traits rely on the same resource, trait values for one adaptively plastic trait might be unavoidably associated with maladaptive trait values for other traits. I address this problem in three traits of Pieris rapae L. (the small cabbage white butterfly) that all rely on the pigment melanin and are adaptively plastic, but have very different functions: wing pattern, immune defense, and pupal color. Cool, short-day rearing conditions simultaneously increased total wing melanization and decreased a melanin-based immune response in females, consistent with predictions. However, cool, short days also reduced the melanin-based immune response in males, despite little effect on male wing melanization. Furthermore, contrary to predictions, these patterns were not altered by differences in dietary resources. Finally, dark-colored rearing backgrounds during pupation substantially increased pupal melanization in both sexes, but was not associated with differences in wing melanization. These results offer only mixed support for the hypothesis of melanin-based trade offs as a source of phenotypic costs to adaptive plasticity in these traits. However, patterns of sexual dimorphism for these traits suggest trade offs might be at work at another level: relative to males, females have consistently more heavily melanized wings but less heavily melanized pupae and immune responses. The reduced immune response under cool, short-day conditions may also have implications for the evolutionary ecology of these butterflies.     

Melanin-based plumage coloration and flight displays in plovers and allies

Plovers and their allies exhibit an impressive diversity of melanin-based plumage patterns ranging from non-melanized to completely melanized species. We use phylogenetic comparative methods to test whether melanization has evolved in relation to sexual selection for attracting mates, to selection for signalling territory defence, or to natural selection for camouflage. First, according to sexual-selection theory, melanized plumage has evolved to amplify the courtship displays of males. As predicted by this hypothesis, we found that males with aerial displays had more melanized plumage than males of ground-displaying species. In addition, sexual dimorphism in melanization was greater in species with display flights than in species with ground displays. Second, melanization may have evolved through social interactions to signal competitive ability in territory defence. We did not find evidence for this hypothesis, since breeding density was unrelated to the melanization of either sex. Finally, melanized plumage may camouflage the incubating parent. The latter hypothesis was not supported, since melanization was unrelated either to the darkness of nest substrate or the extent of vegetation cover. Taken together, our results are most consistent with the sexual-selection hypothesis, and suggest that melanized plumage has evolved to enhance the aerial displays of male plovers.     

Multivariate heredity of melanin-based coloration,body mass and immunity

The genetic covariation among different traits may cause the appearance of correlated response to selection on multivariate phenotypes. Genes responsible for the expression of melanin-based color traits are also involved in other important physiological functions such as immunity and metabolism by pleiotropy, suggesting the possibility of multivariate evolution. However, little is known about the relationship between melanin coloration and these functions at the additive genetic level in wild vertebrates. From a multivariate perspective, we simultaneously explored inheritance and selection of melanin coloration, body mass and phytohemagglutinin (PHA)-mediated immune response by using long-term data over an 18-year period collected in a wild population of the common kestrel Falco tinnunculus. Pedigree-based quantitative genetic analyses showed negative genetic covariance between melanin-based coloration and body mass in male adults and positive genetic covariance between body mass and PHA-mediated immune response in fledglings as predicted by pleiotropic effects of melanocortin receptor activity. Multiple selection analyses showed an increased fitness in male adults with intermediate phenotypic values for melanin color and body mass. In male fledglings, there was evidence for a disruptive selection on rump gray color, but a stabilizing selection on PHA-mediated immune response. Our results provide an insight into the evolution of multivariate traits genetically related with melanin-based coloration. The differences in multivariate inheritance and selection between male and female kestrels might have resulted in sexual dimorphism in size and color. When pleiotropic effects are present, coloration can evolve through a complex pathway involving correlated response to selection on multivariate traits.     

Sexual selection of multiple handicaps in the red-collared widowbird: female choice of tail length but not carotenoid display

Although sexual selection through female choice explains exaggerated male ornaments in many species, the evolution of the multicomponent nature of most sexual displays remains poorly understood. Theoretical models suggest that handicap signaling should converge on a single most informative quality indicator, whereas additional signals are more likely to be arbitrary Fisherian traits, amplifiers, or exploitations of receiver psychology. Male nuptial plumage in the highly polygynous red-collared widowbird (Euplectes ardens) comprises two of the commonly advocated quality advertisements (handicaps) in birds: a long graduated tail and red carotenoid coloration. Here we use multivariate selection analysis to investigate female choice in relation to male tail length, color (reflectance) of the collar, other aspects of morphology, ectoparasite load, display rate, and territory quality. The order and total number of active nests obtained are used as measures of male reproductive success. We demonstrate a strong female preference and net sexual selection for long tails, but marginal or no effects of color, morphology, or territory quality. Tail length explained 47% of male reproductive success, an unusually strong fitness effect of natural ornament variation. Fluctuating tail asymmetry was unrelated to tail length, and had no impact on mating success. For the red collar, there was negative net selection on collar area, presumably via its negative relationship with tail length. None of the color variables (hue, chroma, and brightness) had significant selection differentials, but a partial effect (selection gradient) of chroma might represent a color preference when tail length is controlled for. We suggest that the red collar functions in male agonistic interactions, which has been strongly supported by subsequent work. Thus, female choice targets only one handicap, extreme tail elongation, disregarding or even selecting against the carotenoid display. We discuss whether long tails might be better indicators of genetic quality than carotenoid pigmentation. As regards the evolution of multiple ornaments, we propose that multiple handicap signaling is stable not because of multiple messages but because of multiple receivers, in this case females and males.     

Interpreting melanin-based coloration through deep time: a critical review

Colour, derived primarily from melanin and/or carotenoid pigments, is integral to many aspects of behaviour in living vertebrates, including social signalling, sexual display and crypsis. Thus, identifying biochromes in extinct animals can shed light on the acquisition and evolution of these biological traits. Both eumelanin and melanin-containing cellular organelles (melanosomes) are preserved in fossils, but recognizing traces of ancient melanin-based coloration is fraught with interpretative ambiguity, especially when observations are based on morphological evidence alone. Assigning microbodies (or, more often reported, their ‘mouldic impressions’) as melanosome traces without adequately excluding a bacterial origin is also problematic because microbes are pervasive and intimately involved in organismal degradation. Additionally, some forms synthesize melanin. In this review, we survey both vertebrate and microbial melanization, and explore the conflicts influencing assessment of microbodies preserved in association with ancient animal soft tissues. We discuss the types of data used to interpret fossil melanosomes and evaluate whether these are sufficient for definitive diagnosis. Finally, we outline an integrated morphological and geochemical approach for detecting endogenous pigment remains and associated microstructures in multimillion-year-old fossils.     

Thermal environment shapes cuticle melanism and melanin-based immunity in the ground cricket Allonemobius socius

The thermal melanin hypothesis posits that ectothermic individuals of larger size or from colder environments exhibit darker cuticles due to melanin’s efficacy in absorbing solar radiation. However, melanin is also a crucial component of arthropod immunity. Thus, thermal selection for increased cuticle darkness may profoundly influence melanin-based immune function. In this study, we address the relationships between the thermal environment (season length), cuticular melanism and two aspects of melanin-based immunity across nine thermally distinct populations of the cricket Allonemobius socius. We found that season length (i.e. degree days) and body size had a positive association with cuticle melanism in both sexes across populations, supporting the thermal melanism hypothesis. Despite their smaller size, males were found to have darker cuticles and superior melanin-based immunity. This pattern may be the result of additional selection on males due to sex-specific temperature-dependent activities, such as male calling song. Perhaps most interestingly, we found that short season length populations (i.e. colder) exhibited a greater phenoloxidase activity (aspect of the melanin-based immune system) in addition to darker cuticles in both sexes. This pattern is consistent with direct thermal selection on cuticular color, coupled with indirect selection on melanin-based immunity due to pleiotropy. Thus, thermal selection on cuticle darkness appears to indirectly shape the evolution of pathogen resistance in this system, and potentially for other terrestrial arthropod systems whose ranges encompass a significant thermal gradient.     

Dietary mineral content influences the expression of melanin-based ornamental coloration

Many animals develop bold patches of black or brown colorationthat are derived from melanin pigments and serve as sexual orsocial signals. At present, there is much debate among behavioralecologists over whether melanin-based color signals are costlyto produce. Studies that have manipulated crude aspects of nutrition(i.e., total food intake) or health have generally found melanin-basedplumage ornaments to be less responsive to such factors thanother types of extravagant color (e.g., carotenoid or structuralbased). However, a recently advanced hypothesis argues thatlimited minerals in the diet, such as calcium (Ca), zinc (Zn),and iron (Fe), may serve to increase melanin pigment productionand maintain signal honesty. Here, I experimentally tested whethervariation in the calcium content of the diet affects the colorand extent of melanin-based plumage in male zebra finches (Taeniopygiaguttata). Calcium supplementation increased the size, but notdarkness, of the black breast plumage patch in fledgling andadult males; however, sexually selected, carotenoid-based redbeak coloration was not affected by the diet manipulation. Theseresults are the first to support the idea that acquisition ofminerals from the diet is a unique, limiting factor for theexpression of ornamental melanin coloration in animals.     

Why do curly tail lizards (genus Leiocephalus) curl their tails? An assessment of displays toward conspecifics and predators

Animal display behaviors are used to convey specific messages to other animals, including potential mates, rivals, and predators. However, because these different types of interactions can be mediated by a single behavioral display, or conversely, multiple signals can be used to convey one specific message, interpretation of any particular behavioral display can be difficult. Leiocephalus lizards (i.e., curly tails) provide an excellent opportunity to study the use of display behaviors across multiple contexts. Previous research has demonstrated that the use of tail curling in these lizards is associated with predation risk, but less is known regarding the use of this behavior in social interactions with conspecifics. The goal of this study was to determine the extent to which tail curling display behavior is used to mediate both social and predatory interactions in two species, Leiocephalus barahonensis and L. carinatus. We found that in lizards of both species, tail curling was used in interactions with both conspecifics and potential (human) predators. However, tail curl intensity did not differ between lizards involved in social encounters and solitary lizards, although L. barahonensis lizards performed more headbobs during social than non‐social observations. Further, L. carinatus lizards exhibited greater intensity of tail curling upon fleeing from a human predator than during observations in which individuals interacted with conspecifics, and lizards that exhibited tighter tail curls fled from predators for a longer distance. Finally, tail curl intensity was not correlated with headbob displays in either species, suggesting that these two components of display communicate different information. Our results suggest that tail curling displays, while consistently a component of interactions with potential predators, are not a necessary component of social interactions. These data contribute to a more complete understanding of how and why visual signals evolve for use in communication across multiple contexts.     

Melanins, metals, and mate quality

Many animals display large patches of black or brown color in their integument, which contain melanin pigments and function as important sexually selected indicators of mate quality. To date, however, the particular means by which melanin-based color ornaments are costly to produce and serve as honest advertisements have remained elusive. Here, I propose a novel biochemical mechanism by which melanin-based coloration may serve as a reliable indicator of quality, involving the interplay of metal ions. In animals and other biochemical systems, a series of scarce macro- and microminerals (e.g. Ca, Zn, Cu, Fe) obtained from the diet act as critical regulatory factors in the biosynthesis of eumelanin and phaeomelanin pigments, but can also be toxic to the body when accumulated in high concentrations. As large polymers with many functional (carboxyl) groups, melanin granules also bind these metals and store them in pigmented cells. Thus, by sequestering large deposits of melanin, often in dead tissue (as in hair or feathers), animals may directly reveal dietary access to these rare elements and the physiological protection they have afforded themselves from initially beneficial, but eventually damaging, high mineral concentrations .     

Interactive effects of sex and temperature on locomotion in reptiles

Males and females from several animal taxa differ in locomotorperformance traits such as sprinting and jumping. These performancedimorphisms may be explained at least partially by sexual differencesin physiology or morphology. In ectotherms such as reptiles,however, thermal ecology places an additional constraint onrealized locomotor performance. I review recent studies on reptilesexamining sexual differences in locomotor capacity and relatedthermoregulatory behavior, and discuss potential causes, constraints,and selective pressures that might drive intersexual divergencein capacity for locomotor performance in reptiles. In severalcases where such differences occur, sexual dimorphisms in bodysize do not account for all the observed variation in performance.However, while sex-specific locomotor capacities might be evidentin the laboratory, ecological performance in nature is likelythe result of complex interactions among sex, thermal sensitivity,habitat type, and behavioral locomotor compensation. Resultsfrom laboratory studies of dimorphisms in maximum locomotorcapacity are therefore likely to be poor predictors of realizedecological differences in performance. Nonetheless, sex differencesin performance are potentially important modifiers of male andfemale behavioral strategies and overall fitness, and consequentlyare deserving of more attention than they have thus far received.     

Female choice for male motor skills

Sexual selection was proposed by Darwin to explain the evolution of male sexual traits such as ornaments and elaborate courtship displays. Empirical and theoretical studies have traditionally focused on ornaments; the reasons for the evolution of elaborate, acrobatic courtship displays remain unclear. We addressed the hypothesis that females choose males on the basis of subtle differences in display performance, indicating motor skills that facilitate survival. Male golden-collared manakins (Manacus vitellinus) perform elaborate, acrobatic courtship displays. We used high-speed cameras to record the displays of wild males and analysed them in relation to male reproductive success. Females preferred males that performed specific display moves at greater speed, with differences of tens of milliseconds strongly impacting female preference. In additional males, we recorded telemetrically the heart rate during courtship using miniature transmitters and found that courtship is associated with profoundly elevated heart rates, revealing a large metabolic investment. Our study provides evidence that females choose their mates on the basis of subtle differences in motor performance during courtship. We propose that elaborate, acrobatic courtship dances evolve because they reflect motor skills and cardiovascular function of males.     

RUNAWAY SEXUAL SELECTION LEADS TO GOOD GENES

Mate choice and sexual displays are widespread in nature, but their evolutionary benefits remain controversial. Theory predicts these traits can be favored by runaway sexual selection, in which preference and display reinforce one another due to genetic correlation; or by good genes benefits, in which mate choice is advantageous because extreme displays indicate a well‐adapted genotype. However, these hypotheses are not mutually exclusive, and the adaptive benefits underlying mate choice can themselves evolve. In particular, examining how and why sexual displays become indicators of good genes is challenging in natural systems. Here, we use experimental evolution in “digital organisms” to demonstrate the origins of condition‐dependent indicator displays following their spread due to a runaway process. Surprisingly, handicap‐like costs are not necessary for displays to become indicators of male viability. Instead, a pleiotropic genetic architecture underlies both displays and viability. Runaway sexual selection and good genes benefits should thus be viewed as interacting mechanisms that reinforce one another.     

Evolution of plumage coloration in the crow family (Corvidae) with a focus on the color-producing microstructures in the feathers: a comparison of eight species

Plumage coloration has been the subject for a variety of questions that comprise the center of modern evolutionary biology. Unlike carotenoids that the concentration directly influences the intensity of the color, melanin, in addition to produce brown or black colors, is often involved in producing the structural coloration such as glossiness or iridescence. As the melanin granules can be located in the barbs or the barbules, we aim to (i) discern if the colors observed at macro scale comes from the barbs, the barbules or both in a series of related species and (ii) estimate the evolutionary history of the color-producing mechanisms in the family Corvidae that are known to have melanin-based coloration. From a preliminary comparative analysis on eight representative species, we found three coloration schemes in Corvidae; (1) matte colors of brown or black that were produced in barbs and barbules; (2) non-iridescent structural colors such as blue, bluish gray and white, that were produced in the barbs and (3) iridescent structural colors that were produced only in distal barbules. Comparative character analysis of these coloration schemes suggests that the ancestral state among these species were the colors produced in the barbs and that the color produced in the distal barbules is a derived character. The evolution of iridescence seems tightly linked to the evolution of the colors produced in the distal barbules. Data from more species should be incorporated in order to grasp a full picture on the evolutionary history of plumage coloration in this group of birds.     

Tail Length and Mutual Mate Choice in Bearded Tits (Panurus biarmicus)

Direct sexual selection via mutual mate choice can result in both sexes showing conspicuous traits. We experimentally tested whether this hypothesis can explain tail length in the bearded tit (Panurus biarmicus). In this species, both sexes have a long, graduated tail. Males have, however, a longer tail than females, suggesting perhaps that females are choosier than males in selecting mates. We used two choice set‐ups for each sex: shortened vs. control tail individuals and elongated vs. control tail individuals. We found that direct sexual selection seems to operate differently in the two sexes. In both set‐ups, females spent more time with the male with the longest tail, and they also showed sexual display behaviour only towards these males. Males spent more time with control than with short‐tailed females, but they did not discriminate between control and long‐tailed females. Moreover, males displayed preference towards both short‐ and long‐tailed females. Thus, females preferred long‐tailed males, whereas males did not always prefer long‐tailed females. Our study suggests that mutual mate choice has played a role in the evolution of long tails in bearded tits. It also suggests that the sexual dimorphism in tail length has evolved because mate choice exerts a stronger sexual selection pressure on males than on females.     

Melanin coloration in New World orioles I: carotenoid masking and pigment dichromatism in the orchard oriole complex

Carotenoids produce the brilliant red, orange, and yellow colors of many animals. However, melanin pigments can also confer some of these same hues. Because carotenoid and melanin colors are produced in different ways and may serve different signaling functions, either within or between species, it is important to establish whether one or both types of pigment are responsible for coloration. We have discovered what appears to be an evolutionary switch from carotenoid- to melanin-based color in two sexually dichromatic New World orioles. Using a combination of reflectance spectrometry and chromatographic analyses of plumage pigments, we found that the chestnut plumage of adult male orchard orioles Icterus spurius is produced predominantly by phaeomelanins. Orchard oriole feathers also contain carotenoids, which appear to be masked by the high concentration of phaeomelanins. In contrast, both carotenoids and phaeomelanins appear to contribute to color in adult male Fuertes's orioles I. fuertesi . Moreover, yellow yearling male and female plumage in both species is produced by carotenoids alone. The masking of carotenoids with phaeomelanins in orchard orioles is interesting in light of the signaling roles that carotenoids are thought to play. In addition, these plumage differences produce a unique case of age and sexual pigment dimorphism in orchard and Fuertes's orioles.     

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

Background

In 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 Findings

Three 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/Significance

These 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.     

Variation in context‐dependent foraging behavior across pollinators

Pollinator foraging behavior has direct consequences for plant reproduction and has been implicated in driving floral trait evolution. Exploring the degree to which pollinators exhibit flexibility in foraging behavior will add to a mechanistic understanding of how pollinators can impose selection on plant traits. Although plants have evolved suites of floral traits to attract pollinators, flower color is a particularly important aspect of the floral display. Some pollinators show strong innate color preference, but many pollinators display flexibility in preference due to learning associations between rewards and color, or due to variable perception of color in different environments or plant communities. This study examines the flexibility in flower color preference of two groups of native butterfly pollinators under natural field conditions. We find that pipevine swallowtails (Battus philenor) and skippers (family Hesperiidae), the predominate pollinators of the two native Texas Phlox species, Phlox cuspidata and Phlox drummondii, display distinct patterns of color preferences across different contexts. Pipevine swallowtails exhibit highly flexible color preferences and likely utilize other floral traits to make foraging decisions. In contrast, skippers have consistent color preferences and likely use flower color as a primary cue for foraging. As a result of this variation in color preference flexibility, the two pollinator groups impose concordant selection on flower color in some contexts but discordant selection in other contexts. This variability could have profound implications for how flower traits respond to pollinator‐mediated selection. Our findings suggest that studying dynamics of behavior in natural field conditions is important for understanding plant–pollinator interactions.     

The evolution of sexually dimorphic tail feathers is not associated with tail skeleton dimorphism

Sexual selection can influence the evolution of sexually dimorphic exaggerated display structures. Herein, we explore whether such costly ornamental integumentary structures evolve independently or if they are correlated with phenotypic change in the associated skeletal system. In birds, elongate tail feathers have frequently evolved in males and are beneficial as intraspecific display structures but impart a locomotor/energetic cost. Using the sexually dimorphic tail feathers of several passeriform species as a model system, we test the hypothesis that taxa with sexually dimorphic tail feathers also exhibit sexual dimorphism in the caudal skeleton that supports the muscles and integument of the tail apparatus. Caudal skeletal morphology is quantified using both geometric morphometrics and linear morphometrics across four sexually dimorphic passeriform species and four closely related monomorphic species. Sexual dimorphism is assessed using permutational MANOVA. Sexual dimorphism in caudal skeletal morphology is found only in those taxa that exhibit active functional differences in tail use between males and females. Thus, dimorphism in tail feather length is not necessarily correlated with the evolution of caudal skeletal dimorphism. Sexual selection is sufficient to generate phenotypic divergence in integumentary display structures between the sexes, but these change are not reflected in the underlying caudal skeleton. This suggests that caudal feathers and bones evolve semi‐independently from one another and evolve at different rates in response to different types of selective pressures.     

Sexual Dimorphism in Melanin Pigmentation,Feather Coloration and Its Heritability in the Barn Swallow (Hirundo rustica)

Melanin is the main pigment in animal coloration and considerable variation in the concentrations of the two melanin forms (pheo- and eumlanin) in pigmented tissues exists among populations and individuals. Melanin-based coloration is receiving increasing attention particularly in socio-sexual communication contexts because the melanocortin system has been hypothesized to provide a mechanistic basis for covariation between coloration and fitness traits. However, with few notable exceptions, little detailed information is available on inter-individual and inter-population variation in melanin pigmentation and on its environmental, genetic and ontogenetic components. Here, we investigate melanin-based coloration in an Italian population of a passerine bird, the barn swallow (Hirundo rustica rustica), its sex- and age-related variation, and heritability. The concentrations of eu- and pheomelanin in the throat (brown) and belly (white-to-brownish) feathers differed between sexes but not according to age. The relative concentration of either melanin (Pheo:Eu) differed between sexes in throat but not in belly feathers, and the concentrations in males compared to females were larger in belly than in throat feathers. There were weak correlations between the concentrations of melanins within as well as among plumage regions. Coloration of belly feathers was predicted by the concentration of both melanins whereas coloration of throat feathers was only predicted by pheomelanin in females. In addition, Pheo:Eu predicted coloration of throat feathers in females and that of belly feathers in males. Finally, we found high heritability of color of throat feathers. Melanization was found to differ from that recorded in Hirundo rustica rustica from Scotland or from H. r. erythrogaster from North America. Hence, present results show that pigmentation strategies vary in a complex manner according to sex and plumage region, and also among geographical populations, potentially reflecting adaptation to different natural and sexual selection regimes, and that some coloration components seem to be highly heritable.