A PHYLOGENETIC PERSPECTIVE ON THE EVOLUTION OF SEXUAL DICHROMATISM IN TANAGERS (THRAUPIDAE): THE ROLE OF FEMALE VERSUS MALE PLUMAGE

The evolution of sexual dichromatism in tanagers (family Thraupidae) was studied from a phylogenetic perspective using a molecular-based phylogeny. Mapping patterns of sexual dimorphism in plumage onto the phylogeny reveals that changes in female plumage occur more frequently than changes in male plumage. Possible explanations for this pattern include sexual selection acting on female plumage and natural selection for background matching. The results of this study and other recent phylogenetic and comparative studies suggest that factors affecting female plumage are important in shaping patterns of sexual dimorphism.     

Do bright colors at nests incur a cost due to predation?

Summary Birds show much interspecific variation in the coloration and brightness of their plumage. I examine the hypothesis that selection due to predation on incubating birds and their nest contents can explain part of this diversity. First, I argue that rather than using absolute rates of nest predation to make predictions about the costs of conspicuous colours, we should measure experimentally whether increases in plumage conspicuousness elevate rates of nest predation. Second, I present experimental data investigating the cost of red and brown colour at ground and tree nests. These data provide the first evidence that bright colours do attract predators to nests and that, in addition, this cost varies according to the nesting site. Natural selection seems to most strongly oppose the evolution of conspicuous colours in ground-nesting birds.     

Evolution of sexual dichromatism in relation to nesting habits in European passerines: a test of Wallace's hypothesis

Wallace proposed in 1868 that natural rather than sexual selection could explain the striking differences in avian plumage dichromatism. Thus, he predicted that nesting habits, through their association with nest predation, could drive changes in sexual dichromatism by enabling females in cavity nesters to become as conspicuous as males, whereas Darwin (1871, The Descent of Man and Selection in Relation to Sex, John Murray, London) argued that sexual selection was the sole explanation for dichromatism. Sexual dichromatism is currently used as indicating the strength of sexual selection, and therefore testing Wallace's claim with modern phylogentically controlled methodologies is of prime interest for comparing the roles of natural and sexual selection in affecting the evolution of avian coloration. Here, we have related information on nest attendance, sexual dichromatism and nesting habits (open and cavity nesting) to male and female plumage conspicuousness in European passerines. Nest incubation attendance does not explain male or female plumage conspicuousness but nest type does. Moreover, although females of monochromatic and cavity nesting species are more conspicuous than females of other species, males of monochromatic and open nesting species are those with more cryptic plumage. Finally, analyses of character evolution suggest that changes in nesting habits influence the probability of changes in both dichromatism and plumage conspicuousness of males but do not significantly affect those in females. These results strongly suggest a role of nesting habits in the evolution of plumage conspicuousness of males, and a role for sexual selection also in females, both factors affecting the evolution of sexual dichromatism. We discuss our findings in relation to the debate that Darwin and Wallace maintained more than one century ago on the importance of natural and sexual selection in driving the evolution of plumage conspicuousness and sexual dichromatism in birds, and conclude that our results partly support the evolutionary scenarios envisaged by both extraordinary scientists.     

Size dimorphism and avian‐perceived sexual dichromatism in a New Zealand endemic bird,the whitehead Mohoua albicilla

Sex differences in behavior, morphology, and physiology are common in animals. In many bird species, differences in the feather colors of the sexes are apparent when judged by human observers and using physical measures of plumage reflectance, cryptic (to human) plumage dichromatism has also been detected in several additional avian lineages. However, it remains to be confirmed in almost all species whether sexual dichromatism is perceivable by individuals of the studied species. This latter step is essential because it allows the evaluation of alternative hypotheses regarding the signaling and communication functions of plumage variation. We applied perceptual modeling of the avian visual system for the first time to an endemic New Zealand bird to provide evidence of subtle but consistent sexual dichromatism in the whitehead, Mohoua albicilla. Molecular sexing techniques were also used in this species to confirm the extent of the sexual size dimorphism in plumage and body mass. Despite the small sample sizes, we now validate previous reports based on human perception that in male whiteheads head and chest feathers are physically brighter than in females. We further suggest that the extent of sexual plumage dichromatism is pronounced and can be perceived by these birds. In contrast, although sexual dimorphism was also detectable in the mass among the DNA‐sexed individuals, it was found to be less extensive than previously thought. Sexual size dimorphism and intraspecifically perceivable plumage dichromatism represent reliable traits that differ between female and male whiteheads. These traits, in turn, may contribute to honest communication displays within the complex social recognition systems of communally breeding whitehead and other group‐breeding taxa. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Nest shape explains variation in sexual dichromatism in New World blackbirds

Following Charles Darwin, research on sexual dichromatism has long focused on sexual selection driving ornamentation in males. However, Alfred Russel Wallace proposed another explanation – that dichromatism evolves as a result of selection favoring crypsis in incubating females. Many recent studies suggest that evolutionary changes in sexual dichromatism often result from changes in female, in addition to male, plumage, yet the evolutionary mechanisms driving changes in female plumage remain largely unexplained. To test Wallace's hypothesis, we examined variation in sexual dichromatism and nest shape, a proxy for predation risk, among New World blackbirds (Aves: Icteridae). Phylogenetic models reveal an evolutionary correlation between sexual dichromatism and nest exposure. Specifically, we found that transitions in monochromatic lineages with exposed nests toward either concealed nests or dichromatism were common. Although this evidence supports Wallace's hypothesis that female incubation leads to selection for crypsis or concealment, we also found that transitions to monomorphism were common, even in lineages with exposed nests – a result suggestive of a role for positive selection on female ornamentation. These patterns of plumage evolution support a growing body of work emphasizing the importance of developing and testing hypotheses to explain evolutionary changes in female, as well as male, ornamentation.     

Sexual dimorphism and dichromatism in Steere's Liocichla (Liocichla steerii)

ABSTRACT.   Although sexual differences in birds can be extreme, differences between males and females in body size and plumage color are more subtle in many species. We used a genetic-based approach to determine the sex of male and female Steere's Liocichla ( Liocichla steerii ) and examine the degree of size dimorphism and plumage dichromatism in this apparently monomorphic species. We found that males were significantly larger than females. In addition, Steere's Liocichla have a prominent yellow plumage patch on the lores that was significantly larger in males than females for both live birds and museum specimens. We also used reflectance spectrometry to quantify the color of the yellow-green breast feathers of Steere's Liocichla and found no significant differences between males and females in brightness, intensity, saturation, or hue. However, females tended to have brighter breast plumage, particularly at long wavelengths. Collectively, these color variables were useful in discriminating birds according to sex when used in a discriminant function analysis. Our study suggests that sexual selection may be more widespread than once assumed, even among birds considered monomorphic, and emphasizes the need for additional data from tropical and subtropical species.     

Brightness variability in the white badge of the eagle owl Bubo bubo

The application of modern spectrometry to the study of avian colour variability has revealed ignored patterns of colour variation such as male‐biased sexual dichromatism and seasonal variability in the plumage. However, the variation in the achromatic property of such traits, that is in the total light reflectance of the spectrum (i.e., brightness), has commonly been overlooked. The evolution of signals based on brightness should be favoured in those species that are active when light is scarce, i.e. at dawn and dusk. The eagle owl Bubo bubo is monogamous and apparently monomorphic in plumage‐coloration. In this species, sexual and territorial call behaviour is mainly performed at dawn and dusk, during which a white patch on the throat is repeatedly exposed at each call. We measured the total light reflectance of the feathers of this badge in 39 eagle owl specimens from museum collections. We found seasonal variability and sexual dichromatism in the brightness of the plumage badge. The total reflectance of this trait peaked during the territorial‐mating period. Moreover, females showed higher values of brightness than males, in agreement with the reversed body size dimorphism present in this and many other raptor species. Finally, female but not male body size was positively correlated with white badge reflectance.     

Evolution of sexual dichromatism: contribution of carotenoid- versus melanin-based coloration

In birds, carotenoid-based plumage coloration is more dependent on physical condition and foraging abilities and less constrained developmentally than is melanin-based coloration. Thus, female mate choice for honest signals should result in more intense sexual selection on carotenoid- than on melanin-based plumage coloration. Using variation in sexual dimorphism as an indirect measure of the intensity of sexual selection, we tested the prediction mat variation in sexual dimorphism is driven more by change in carotenoid-based coloration between males and females dian by change in melanin-based coloration. Examination of historical changes in carotenoid- versus melanin-based pigmentation in 126 extant species of Cardueline finches supported this prediction. We found that carotenoid-derived coloration changed more frequendy among congeners dian melanin-based coloration. In both sexes, increase in carotenoid-based coloration score, but not in melanin-based coloration score, was strongly associated with increase in sexual dichromatism. In addition, sexual dimorphism in carotenoid-based coloration contributed more to overall dichromatism than dimorphism in melanin-based plumage. Our results supported die hypothesis that melanin-based and carotenoid-based coloration have fundamentally different signal content and suggest that combining melanin-based and carotenoid-based coloration in comparative analyses is not appropriate.     

Brightness variability in the white badge of the eagle owl Bubo bubo

The application of modern spectrometry to the study of avian colour variability has revealed ignored patterns of colour variation such as male-biased sexual dichromatism and seasonal variability in the plumage. However, the variation in the achromatic property of such traits, that is in the total light reflectance of the spectrum (i.e., brightness), has commonly been overlooked. The evolution of signals based on brightness should be favoured in those species that are active when light is scarce, i.e. at dawn and dusk. The eagle owl Bubo bubo is monogamous and apparently monomorphic in plumage-coloration. In this species, sexual and territorial call behaviour is mainly performed at dawn and dusk, during which a white patch on the throat is repeatedly exposed at each call. We measured the total light reflectance of the feathers of this badge in 39 eagle owl specimens from museum collections. We found seasonal variability and sexual dichromatism in the brightness of the plumage badge. The total reflectance of this trait peaked during the territorial-mating period. Moreover, females showed higher values of brightness than males, in agreement with the reversed body size dimorphism present in this and many other raptor species. Finally, female but not male body size was positively correlated with white badge reflectance.     

Different modes of evolution in males and females generate dichromatism in fairy‐wrens (Maluridae)

Sexual dichromatism in birds is often attributed to selection for elaboration in males. However, evolutionary changes in either sex can result in plumage differences between them, and such changes can result in either gains or losses of dimorphism. We reconstructed the evolution of plumage colors in both males and females of species in Maluridae, a family comprising the fairy‐wrens (Malurus, Clytomias, Sipodotus), emu‐wrens (Stipiturus), and grasswrens (Amytornis). Our results show that, across species, males and females differ in their patterns of color evolution. Male plumage has diverged at relatively steady rates, whereas female coloration has changed dramatically in some lineages and little in others. Accordingly, in comparisons against evolutionary models, plumage changes in males best fit a Brownian motion (BM) model, whereas plumage changes in females fit an Ornstein Uhlenbeck (OU) multioptimum model, with different adaptive peaks corresponding to distributions in either Australia or New Guinea. Levels of dichromatism were significantly associated with latitude, with greater dichromatism in more southerly taxa. Our results suggest that current patterns of plumage diversity in fairy‐wrens are a product of evolutionary changes in both sexes, driven in part by environmental differences across the distribution of the family.     

Reversed plumage ontogeny in a female hummingbird: implications for the evolution of iridescent colours and sexual dichromatism

In polygynous birds, bright plumage is typically more extensive in the sexually competitive males and develops at or after sexual maturity. These patterns, coupled with the importance of male plumage in sexual displays, fostered the traditional hypothesis that bright plumages and sexual dichromatism develop through the actions of sexual selection on males. This view remains problematic for hummingbirds, all of which are polygynous, because their bright iridescent plumages are also important non-sexual signals associated with dominance at floral nectar sources. Here I show that female amethyst-throated sunangels [ Heliangelus amethysticollis (d'Orbigny & Lafresnaye)], moult from an immature plumage with an iridescent gorget to an adult plumage with a non-iridescent gorget. This 'reversed' ontogeny contradicts the notion that iridescent plumage has a sexual function because sexual selection in polygynous birds should be lowest among non-reproductive immature females. Moreover, loss of iridescent plumage in adult females indicates that adult sexual dichromatism in H. amethysticollis is due in large part to changes in female ontogeny. I suggest that both the ontogeny and sexual dichromatism evolved in response to competition for nectar.     

CORRELATED EVOLUTION OF MIGRATION AND SEXUAL DICHROMATISM IN THE NEW WORLD ORIOLES (ICTERUS)

The evolution of sexual dimorphism has long been attributed to sexual selection, specifically as it would drive repeated gains of elaborate male traits. In contrast to this pattern, New World oriole species all exhibit elaborate male plumage, and the repeated gains of sexual dichromatism observed in the genus are due to losses of female elaboration. Interestingly, most sexually dichromatic orioles belong to migratory or temperate‐breeding clades. Using character scoring and ancestral state reconstructions from two recent studies in Icterus, we tested a hypothesis of correlated evolution between migration and sexual dichromatism. We employed two discrete phylogenetic comparative approaches: the concentrated changes test and Pagel's discrete likelihood test. Our results show that the evolution of these traits is significantly correlated (CCT: uncorrected P < 0.05; ML: LRT = 12.470, P < 0.005). Indeed, our best model of character evolution suggests that gains of sexual dichromatism are 23 times more likely to occur in migratory taxa. This study demonstrates that a life‐history trait with no direct relationship with sexual selection has a strong influence on the evolution of sexual dichromatism. We recommend that researchers further investigate the role of selection on elaborate female traits in the evolution of sexual dimorphism.     

Sexual dichromatism in the yellow-breasted chat Icteria virens: spectrophotometric analysis and biochemical basis

Sexual dimorphism or dichromatism has long been considered the result of sexual selection. However, for many organisms the degree to which sexual dichromatism occurs has been determined within the confines of human perception. For birds, objective measures of plumage color have revealed previously unappreciated sexual dichromatism for several species. Here we present an unbiased assessment of plumage dichromatism in the yellow-breasted chat Icteria virens . Chats exhibit yellow to orange throat and breast plumage that to the unaided human observer differs only subtly in color. Spectrophotometric analyses revealed that chat throat and breast feathers exhibited reflective curves with two peaks, one in the ultraviolet and one in the yellow end of the spectrum. We found differences in both the shape and magnitude of reflectance curves between males and females. Moreover, for feathers collected from the lower edge and middle of the breast patch, male plumage reflected more light in the ultraviolet and yellow wavelengths compared to females, whereas male throat feathers appeared brighter than those of females only in the ultraviolet. Biochemical analyses indicated that the plumage pigmentation consisted solely of the carotenoid all- trans lutein and we found that males have higher concentrations of plumage carotenoids than females. Feathers that were naturally unpigmented reflected more UV light than yellow feathers, suggesting a potential role of feather microstructure in UV reflectance.     

Covariation of sexual dichromatism and plumage colours in lekking and non-lekking birds: A comparative analysis

The extreme polygyny expressed by male lekking birds leads to the expectation that sexual dimorphism should be greater in lekkers than related non-lekkers. However, evidence for this association is weak, and many lekkers are actually monomorphic in size and plumage. To better understand the kinds of plumages associated with lekking, I characterized plumage variation for combinations of sexual dichromatism and colourfulness-and-conspicuousness (COCO) among lekking and related non-lekking birds. Compared in this way, the plumages of lekkers and non-lekkers differ dramatically for both sexes. Correlations between sexual dichromatism and COCO for phylogenetically independent contrasts are significant for male lekkers (positive) and female non-lekkers (negative), but not for female lekkers or male non-lekkers. Moreover, the total number of character–state combinations, and multivariate measures of variability, are greater in non-lekkers than lekkers.The characteristic plumages of lekkers (duller monochromatic, brighter dichromatic and intermediate between these extremes) comprise just a subset of those observed among non-lekkers, and exclude extremely dull dichromatic and extremely bright monochromatic plumages. I suggest that predation, and foraging behaviours compatible with lekking, may restrict plumage variation among lekkers. Thus ecological rather than overt sexual characteristics may explain monomorphism in birds under intense mate competition, as well as the paradox of strong female mate preferences on leks, where males appear to contribute only sperm to female reproductive efforts.     

Melanin‐based sexual dichromatism in the Western Palearctic avifauna implies darker males and lighter females

Melanins are the most common pigments providing coloration in the plumage and bare skin of birds and other vertebrates. Numerous species are dichromatic in the adult or definitive plumage, but the direction of this type of sexual dichromatism (i.e. whether one sex tends to be darker than the other) has not been thoroughly investigated. Using color plates, we analysed the presence of melanin‐based color patches in 666 species belonging to 69 families regularly breeding in the Western Palearctic. Sexual dichromatism based on melanins in at least one integumentary part involved 205 (30.7%) species. The body parts contributing more frequently to dichromatism were the dorsal areas, head and breast, whereas the less dichromatic body parts were the belly and the exposed integumentary parts (i.e. bill and legs). Regarding the phylogenetic spread of dichromatisms, 37 (53.6%) families contained at least one species with melanin‐based sexual dimorphism in the definitive adult plumage. As for the direction of the color difference, males are darker than females in a majority of species, meaning that males tend to produce more eumelanin and females tend to synthesize more pheomelanin. This survey has revealed the high prevalence of melanins in the emergence of sexual dichromatism in birds, at least in the Western Palearctic. Whether the described pattern is due to sexual selection promoting more conspicuous males or to natural selection for more cryptic females remains to be determined. Given that pheomelanin synthesis concurrently consumes the antioxidant glutathione but may also reduces toxic cysteine, sex‐biased physiological factors should also be given consideration in the evolution of bird plumages.     

THE EVOLUTION OF PLUMAGE BRIGHTNESS IN BIRDS IS RELATED TO EXTRAPAIR PATERNITY

A positive association between plumage brightness of male birds and the degree of polygyny may be the result of sexual selection. Although most birds have a socially monogamous mating system, recent paternity analyses show that many offspring are fathered by nonmates. Extrapair paternity arises from extrapair copulations which are frequently initiated by females. Not all females will be able to mate with a male of the preferred phenotype, because of the mating decisions of earlier paired females; extrapair copulations may be a means for females to adjust their precopulation mate choice. We use two comparative analyses (standardized linear contrasts and pairwise comparisons between closely related taxa) to test the idea that male plumage brightness is related to extrapair paternity. Brightness of male plumage and sexual dimorphism in brightness were positively associated with high levels of extrapair paternity, even when potentially confounding variables were controlled statistically. This association between male brightness and extrapair paternity was considerably stronger than the association between male brightness and the degree of polygyny. Cuckoldry thus forms an important component of sexual selection in birds.     

Cryptic sexual dichromatism occurs across multiple types of plumage in the Green-backed Tit Parus monticolus

Several recent studies have found instances of cryptic sexual dichromatism within avian taxa. Although this dichromatism has been found in plumage produced through a variety of proximate mechanisms, little is known about how dichromatism varies across these types of plumage within a single species. We used a reflectance spectrometer to measure colour within the Green-backed Tit Parus monticolus , a species which displays multiple types of pigment and structural colours. We found significant differences in spectral measurements corresponding to hue, chroma, and brightness between male and female carotenoid, melanin, structural white, grey and structural blue plumage. The only plumage that did not appear to show sexual dichromatism was the olive plumage of the back. These findings suggest that the mechanism(s) producing cryptic dichromatism in the Green-backed Tit are non-specific and act across multiple types of plumage, rather than within a single type, such as carotenoid-based or structurally produced.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

The role of sexual and natural selection in shaping patterns of sexual dichromatism in the largest family of songbirds (Aves: Thraupidae)

Males and females can be under different evolutionary pressures if sexual and natural selection is differentially operating in each sex. As a result, many species have evolved sexual dichromatism, or differences in coloration between sexes. Although sexual dichromatism is often used as an index of the magnitude of sexual selection, sexual dichromatism is a composite trait. Here, we examine the evolution of sexual dichromatism in one of the largest and most ecologically diverse families of birds, the tanagers, using the avian visual perspective and a species‐level phylogeny. Our results demonstrate that the evolutionary decreases of sexual dichromatism are more often associated with larger and more frequent changes in male plumage coloration, and evolutionary increases are not more often associated with larger changes in either sex. Furthermore, we show that the crown and ventral plumage regions are correlated with sexual dichromatism in males, and that only male plumage complexity is positively correlated with sexual dichromatism. Finally, we demonstrate that light environment is important in shaping both plumage brilliance and complexity. By conducting a multilevel analysis of plumage evolution in males and females, we show that sexual dichromatism evolves via a mosaic of sexual and natural selection in both sexes.     

RECONSTRUCTING THE EVOLUTION OF SEXUAL DICHROMATISM: CURRENT COLOR DIVERSITY DOES NOT REFLECT PAST RATES OF MALE AND FEMALE CHANGE

Males of sexually dimorphic species often appear more divergent among taxa than do females, so it is often assumed that evolutionary changes have occurred primarily in males. Yet, sexual dimorphisms can result from historical changes in either or both of the sexes, and few previous studies have investigated such patterns using phylogenetic methods. Here, we describe the evolution of male and female plumage colors in the grackles and allies (Icteridae), a songbird clade with a broad range in levels of sexual dichromatism. Using a model of avian perceptual color space, we calculated color distances within and among taxa on a molecular phylogeny. Our results show that female plumage colors have changed more dramatically than male colors in the evolutionary past, yet male colors are significantly more divergent among species today. Historical increases in dichromatism have involved changes in both sexes, whereas decreases in dichromatism have nearly always involved females evolving rapidly to look like males. Dichromatism is also associated with mating system in this group, with monogamous taxa tending to exhibit relatively low levels of sexual dichromatism. Our findings suggest that, despite appearances, female plumage evolution plays a more prominent role in sexual dichromatism than is generally assumed.