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.     

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.     

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.     

Age differences in blue tit Parus caeruleus plumage colour: within‐individual changes or colour‐biased survival?

In many species of passerine birds yearlings display a less elaborate version of the adult secondary sexual traits, but the causes of such differences in ornamentation are not always well understood. We studied age-related changes in blue tit Parus caeruleus UV/blue structural crown coloration, a sexually selected trait. In our Austrian study population, older blue tits, irrespective of sex, displayed on average a more ultraviolet (lower hue, higher UV chroma), more chromatic and brighter crown coloration than yearlings. This age dichromatism was caused by within-individual changes in the expression of crown coloration between years since males and females became more UV, more chromatic and brighter as they aged. Colour biased survival did not contribute to the observed pattern of age dichromatism since crown coloration was largely unrelated to overwinter survival. Between-year repeatability of crown colour was significant for most colour variables but low in general, and lower for females than for males. In the blue tit, yearling males might benefit from being less ornamented by avoiding adult aggression but at the expense of sexual attractiveness. Adaptive explanations of blue tit age dichromatism should however take into account that age effects were of similar magnitude in males and females. This suggests that both male and female yearlings could benefit from being less ornamented and hence that sexual selection might be acting on both sexes simultaneously in this species.     

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.     

Males in seemingly female‐like plumage do not mimic females: UV reflectance reveals temporal cryptic dimorphism in a manakin species exhibiting delayed plumage maturation

Manakins (Pipridae) are neotropical birds that usually exhibit delayed plumage maturation (DPM). Thus, while plumage of most adult male manakins is brightly conspicuous, subadult males and females are basically dull‐olive green. Although sexual dichromatism in some bird species may be evident only through UV reflectance, this phenomenon, known as hidden sexual dichromatism, has not been previously studied in manakins to compare subadult males and females. Within this framework, we carried out spectrophotometric analyses in searching for hidden sexual dichromatism in the white‐bearded manakin Manacus manacus, through comparison of UV spectra in females and subadult males in green plumage. Our results revealed UV reflectance in both sexes in green plumage. Moreover, we found UV spectral differences in homologous color patches between sexes, particularly at belly. Since the observed differences may allow intraspecific sex recognition of individuals in green plumage, our results do not support the female‐mimicry hypothesis to explain delayed plumage maturation in the white‐bearded manakin. Although our findings dismiss the female mimicry hypothesis, we cannot state whether these results support the non‐mutually exclusive cryptic and status signaling hypotheses. We propose then, that dull coloration of subadult males may serve both as a cryptic trait and to limit the energetic costs of acquiring the adult plumage before sexual maturity. Meanwhile, differential UV color traits between sexes in green plumage may allow adult males to avoid unnecessary energy expenditures in courtship displays in the presence of males near leks, and to selectively focus their the courtship displays on females. In accordance with the status signaling hypothesis, subadult males can be recognized both as males and subordinates and consequently may practice courtship displays without suffering aggressions by adult males. Our results highlight the importance to include a wider range of spectrophotometric information analyses for testing hypotheses regarding delayed plumage maturation.     

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.     

Contemporary divergence of island bird plumage

Although the diversity in avian plumage coloration is striking, there is little known about the rate with which colour diverges. Eastern bluebirds Sialia sialis bermudensis on the island of Bermuda are considered endemic based upon differences in coloration from the mainland, but recent molecular evidence suggests they established on the island only 400 yr ago. We explored sexual dichromatism and colour divergence in this isolated population, thus providing one of the few quantitative accounts of contemporary plumage change. Contrary to expectations that sexual dichromatism would decrease in this sedentary island population, we found that males and females have increased plumage ornamentation in a coordinated fashion that acts to preserve sexual dichromatism, while plumage colour is also altered to become brighter and bluer. These differences were in place at least 100 yr ago based upon a separate analysis of museum specimens. Our results provide insight into the divergence of plumage colour in an incipient species, and we show the remarkable extent to which plumage colour can change over contemporary time frames.     

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.     

Reproductive correlates of plumage coloration of female Mountain Bluebirds

Many studies have shown that the plumage coloration of male birds can act as an honest signal of quality, indicating benefits that a female could gain from pairing with a specific male. In some species, females also display ornamental plumage, but less is known about the function and potential adaptive significance of female coloration because most research has focused on male coloration. Male Mountain Bluebirds (Sialia currucoides) display full body, ultraviolet (UV)‐blue plumage, whereas female plumage is more subdued, with blue color focused on the rump, wing, and tail. During the 2011 and 2012 breeding seasons (May–July) near Kamloops, BC, Canada, we examined coloration of the rump and tail of female Mountain Bluebirds to determine if their plumage could act as an indicator of direct reproductive benefits (e.g., enhanced parental care or reproductive success) to potential mates. We found no relationship between female plumage coloration and either provisioning rate or fledging success. However, female coloration varied with age, with after‐second‐year (ASY) females having brighter, more UV‐blue tail feathers than second‐year (SY) females. In addition, ASY females with brighter, more UV‐blue tails had larger clutches. We also observed positive assortative mating by tarsus length. Because previous work with other species suggests that female body size may be a good predictor of breeding success, males could potentially benefit from pairing with larger females. However, reproductive success did not vary with female size in our study. Although our evidence that structural plumage coloration of female Mountain Bluebirds is a signal of direct reproductive benefits for males (e.g., higher reproductive success) is limited, our results (i.e., ASY females with brighter tails than SY females, and ASY females with brighter tails having larger clutches) do suggest the potential for sexual selection to act on female coloration.     

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.     

Plumage brightness predicts non-breeding season territory quality in a long-distance migratory songbird, the American redstart Setophaga ruticilla

Many species of birds exhibit brilliant ornamental plumage, yet most research on the function and evolution of plumage has been confined to the breeding season. In the American redstart Setophaga ruticilla , a long-distance Neotropical-Nearctic migratory bird, the acquisition of a winter territory in high-quality habitat advances spring departure and subsequent arrival on breeding areas, and increases reproductive success and annual survival. Here, we show that males holding winter territories in high-quality, black mangrove habitats in Jamaica have brighter yellow-orange tail feathers than males occupying territories in poor-quality second-growth scrub habitats. Moreover, males arriving on the breeding grounds from higher-quality winter habitats (inferred by stable-carbon isotopes) also had brighter tail feathers. Because behavioral dominance plays an important role in the acquisition of winter territories, plumage brightness may also be related to fighting ability and the acquisition and maintenance of territories in high-quality habitat. These results highlight the need for further research on the relationships between plumage coloration, behavior, and the ecology of over-wintering migratory birds.     

Light matters: testing the “Light Environment Hypothesis” under intra‐ and interspecific contexts

The “Light Environment Hypothesis” (LEH) proposes that evolution of interspecific variation in plumage color is driven by variation in light environments across habitats. If ambient light has the potential to drive interspecific variation, a similar influence should be expected for intraspecific recognition, as color signals are an adaptive response to the change in ambient light levels in different habitats. Using spectrometry, avian‐appropriate models of vision, and phylogenetic comparative methods, I quantified dichromatism and tested the LEH in both intra‐ and interspecific contexts in 33 Amazonian species from the infraorder Furnariides living in environments with different light levels. Although these birds are sexually monochromatic to humans, 81.8% of the species had at least one dichromatic patch in their plumage, mostly from dorsal areas, which provides evidence for a role for dichromatism in sex recognition. Furthermore, birds from habitats with high levels of ambient light had higher dichromatism levels, as well as brighter, more saturated, and more diverse plumages, suggesting that visual communication is less constrained in these habitats. Overall, my results provide support for the LEH and suggest that ambient light plays a major role in the evolution of color signals in this group of birds in both intra‐ and interspecific contexts. Additionally, plumage variation across light environments for these drab birds highlights the importance of considering ambient light and avian‐appropriate models of vision when studying the evolution of color signals in birds.     

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.     

Selection underlies phenotypic divergence in the insular Azores woodpigeon

The study of phenotypic evolution in island birds following colonization is a classic topic in island biogeography. However, few studies explicitly test for the role of selection in shaping trait evolution in these taxa. Here, we studied the Azores woodpigeon (Columba palumbus azorica) to investigate differences between island and mainland populations, between females and males, and interactions between geographical origin and sex, by using spectrophotometry to quantify plumage colour and linear measurements to examine external and skeletal morphology. We further tested if selection explains the observed patterns by comparing phenotypic differentiation to genome‐wide neutral differentiation. Our findings are consistent with several predictions of morphological evolution in island birds, namely differences in bill, flight and leg morphology and coloration differences between island and mainland birds. Interestingly, some plumage and morphological traits that differ between females and males respond differently according to geographical origin. Sexual dimorphism in colour saturation is more pronounced in the mainland, but this is driven by selection on female plumage coloration. Differences in flight morphology between females and males are also more pronounced in the mainland, possibly to accommodate contrasting pressures between migration and flight displays. Overall, our results suggest that phenotypic differentiation between mainland and island populations leading to divergent sexual dimorphism patterns can arise from selection acting on both females and males on traits that are likely under the influence of natural and sexual selection.     

Broad‐scale variation in sexual dichromatism in songbirds is not explained by sex differences in exposure to predators during incubation

The evolution of sexual dichromatism provoked one of the greatest disagreements between Charles Darwin and Alfred Russel Wallace. According to Darwin the main driving force is sexual selection, whereby choosy females prefer showy males, leading to the evolution of conspicuous male plumage. On the other hand, Wallace suggested that dichromatism may arise because nest predation favors more cryptic females. To test the role of natural selection in the evolution of dichromatism we combined quantitative data on differences in parental share in nest attentiveness (representing the strength of natural selection on males vs females) with spectrophotometric measurements of dichromatism in 412 species of songbirds from 69 families. We expected to find stronger dichromatism in open‐nesting species with more divergent parental roles and in body parts exposed during incubation. Dichromatism was not related to the differences in parental share during incubation, but it was most pronounced in lekking species, migrants, and small species. Our results thus suggest that Wallace's hypothesis is not able to explain broad‐scale variation in the dichromatism of songbirds, but point to a role for sexual selection, mutual mate choice, and migration strategy in shaping the extraordinary variation in dichromatism exhibited by songbirds.     

Selection and inheritance of sexually dimorphic juvenile plumage coloration

Sexually dimorphic plumage coloration is widespread in birds and is generally thought to be a result of sexual selection for more ornamented males. Although many studies find an association between coloration and fitness related traits, few of these simultaneously examine selection and inheritance. Theory predicts that sex‐linked genetic variation can facilitate the evolution of dimorphism, and some empirical work supports this, but we still know very little about the extent of sex linkage of sexually dimorphic traits. We used a longitudinal study on juvenile Florida scrub‐jays (Aphelocoma coerulescens) to estimate strength of selection and autosomal and Z‐linked heritability of mean brightness, UV chroma, and hue. Although plumage coloration signals dominance in juveniles, there was no indication that plumage coloration was related to whether or not an individual bred or its lifetime reproductive success. While mean brightness and UV chroma are moderately heritable, hue is not. There was no evidence for sex‐linked inheritance of any trait with most of the variation explained by maternal effects. The genetic correlation between the sexes was high and not significantly different from unity. These results indicate that evolution of sexual dimorphism in this species is constrained by low sex‐linked heritability and high intersexual genetic correlation.     

Dynamic sexual dichromatism in an explosively breeding Neotropical toad

Sexual selection often promotes the evolution of elaborate colour signals in males, but the importance of sexually selected colour signals remains poorly studied in amphibians. We used reflectance spectrometry to document pronounced sexual dichromatism and dramatic colour change in Bufo luetkenii, a toad that breeds in large aggregations at the onset of the rainy season in Costa Rica. Our observations suggest that males fade rapidly from a vibrant lemon yellow to a dull brown once they have paired with a female. We demonstrate this by showing that males are much brighter than females and that unpaired males are more colourful than males in amplexus. We also show that coloration fades rapidly when males are briefly held captive. This is, to our knowledge, the first study to document such dynamic change in male coloration and sexual dichromatism in anurans.     

Mating status correlates with dorsal brightness in some but not all poison frog populations

Sexual signals are important for intraspecific communication and mate selection, but their evolution may be driven by both natural and sexual selection, and stochastic processes. Strawberry poison frogs (Oophaga pumilio) show strong color divergence among populations, but coloration also varies among individuals of the same population. The importance of coloration for female mate choice has been studied intensely, and sexual selection seems to affect color divergence in strawberry poison frogs. However, the effect of coloration on mating success under field conditions has received very little attention. Furthermore, few studies examined how phenotypic variation among individuals of the same color morph affects mate selection under natural conditions. We measured the spectral reflectance of courting and noncourting individuals and their background substrates in three geographically separated populations. In one population (Sarapiquí, Costa Rica), we found that naturally occurring courting pairs of males and females had significantly brighter dorsal coloration than individual males and females not engaged in courtship interactions. Our field observations suggest that, in the wild, females prefer brighter males while the reason for the higher courtship activity of brighter females remains unclear. Overall our results imply that brightness differences among individuals of the same color morph may actually affect reproductive success in some populations of strawberry poison frogs.     

Reflectance of sexually dichromatic UV‐blue patches varies during the breeding season and between two subspecies of Gallotia galloti (Squamata: Lacertidae)

Body coloration is sexually dimorphic in many vertebrate species, including lizards, in which males are often more conspicuous than females. A detailed analysis of the relative size of coloured patches and their reflectance, including the ultraviolet (UV) range, has rarely been performed. In the present work we quantified sexual dimorphism in body traits and surface area of all lateral patches from adult females and males of two subspecies of Gallotia galloti (G. g. galloti and G. g. eisentrauti). We also analysed the magnitude of sexual dichromatism in the UV‐visible reflectance of such patches and the changes in patch size and brightness during the reproductive season (April–July). Males had significantly larger patch areas (relative to their snout‐vent length) and higher brightness (mainly in the UV‐blue range) than did females in both subspecies. The comparison of relative patch areas among months did not reach statistical significance. However, patch brightness significantly changed during the breeding season: that of the UV‐blue (300–495 nm) range from lizards of the two subspecies was significantly larger in June than in April, while brightness in the 495–700 nm range in G. g. galloti was larger in May, June, and July than in April. A different pattern of dichromatism was also detected in the two populations, with G. g. eisentrauti being more sexually dichromatic than G. g. galloti. We discuss the results in terms of possible evolutionary causes for the sexual dichromatism related to different ecological characteristics of the habitats where each subspecies live. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 556–569.