Natural and sexual selection act on different axes of variation in avian plumage color
Abstract
The bright colors of birds are often attributed to sexual selection on males, but in many species both sexes are colorful and it has been long debated whether sexual selection can also explain this variation. We show that most evolutionary transitions in color have been toward similar plumage in both sexes, and the color of both sexes (for example, bright or dull) was associated with indices of natural selection (for example, habitat type), whereas sexual differences in color were primarily associated with indices of sexual selection on males (for example, polygyny and large testes size). Debate about the evolution of bird coloration can be resolved by recognizing that both natural and sexual selection have been influential, but they have generally acted on two different axes: sexual selection on an axis of sexual differences and natural selection on both sexes for the type of color (for example, bright or dull).
INTRODUCTION
Sexual dichromatism in birds has provided a model system for understanding sexual (1) and natural (2) selection and their roles in speciation (3). For example, Darwin’s (4) theory of sexual selection was based on his observations of the bright colors of males, which he thought were preferred by females and led to a mating advantage for more colorful males. Wallace, on the other hand, pointed out that in many species, females are as “gay and brilliant” as the male, and he suggested that dichromatism evolved as a consequence of nest predation favoring more cryptic females (5). Debate over the evolution of plumage color continues to this day with evidence for both natural (6, 7) and sexual (8, 9) selection acting on plumage color. Part of the controversy may be related to two main limitations of our understanding of plumage color evolution.
First, most studies have examined differences in color between the sexes without quantifying the color of males and females separately. As the debate between Darwin and Wallace illustrates, it is necessary to know if males are becoming brighter or females duller to determine how evolution has produced dichromatism (9, 10). Second, the focus on sexual dichromatism limits our ability to determine how and why monochromatism arises. For example, why are both sexes colorful or both dull? Evolutionary transitions to monochromatism may actually be more common than transitions to dichromatism (11, 12), but it is not known what factors produce these changes in plumage.
Both dichromatism and monochromatism can be produced by natural and sexual selection. For example, dichromatism is often greater in species with stronger sexual selection, as indexed by mating system (for example, polygyny) (9); however, natural selection could also favor dichromatism, if the risk of nest predation favors duller plumage in females than males (Wallace’s hypothesis). Similarly, monochromatism may be favored by sexual (or social) selection if bright plumage in both sexes helps them choose mates or compete intrasexually for territories or other resources (13). Natural selection could also favor monochromatism if both sexes provide parental care and dull plumage in both sexes increases crypsis and, consequently, reduces nest predation. Thus, the extent of dichromatism could be correlated with indices of sexual or natural selection, but we might expect the color (brightness and hue) of both sexes to be primarily correlated with indices of natural selection, such as predation risk, because they are more likely to affect both sexes.
Thus, a comprehensive understanding of plumage color will require analysis of all types of plumage change in each sex. Here, we examined both male and female plumage color in relation to 10 indices of natural and sexual selection to test whether dichromatism was primarily due to sexual selection, as Darwin (4) proposed, whereas the color of both sexes (for example, whether both sexes were dull or bright) was primarily due to natural selection.
RESULTS
Color variation within and between the sexes
We used museum specimens to measure the reflectance spectra (320 to 700 nm) of male and female breeding plumage in a worldwide sample of 977 species (~10% of all species) representing at least 79% of avian orders (data file S1). Most (97%) of the variation in plumage reflectance were described by the first (PC1; 91%) and second (PC2; 6%) principal components, which correspond to brightness and hue, respectively (table S1). Across species, males increased in brightness (Fig. 1A) and hue (Fig. 1C) at a greater rate than did females in phylogenetic regressions. However, there was often more variation in plumage color within a sex than between them (that is, dichromatism; N = 977 species). For example, variation in male brightness (PC1 scores; SD = 13.2; variance ratio test, F976,976 = 5.26, P < 0.001) and female brightness (SD = 12.1; F976,976 = 4.4, P < 0.001) were both greater than variation in brightness between the sexes (that is, dichromatism; SD = 5.8). There was also greater variation in male hue (SD = 4.2) than in sexual dichromatism in hue (SD = 3.1; F976,976 = 1.86, P < 0.001). On the other hand, female hue (SD = 2.8) was not more variable than sexual dichromatism in hue (SD = 3.1; F976,976 = 0.86, P = 0.99).
Fig. 1 Brightness (A) and hue (C) of males and females are strongly correlated in phylogenetic reduced major axis (RMA) regressions of PC scores (red lines).
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