Sexual selection predicts the rate and direction of colour divergence in a large avian radiation

Abstract

Sexual selection is proposed to be a powerful driver of phenotypic evolution in animal systems. At macroevolutionary scales, sexual selection can theoretically drive both the rate and direction of phenotypic evolution, but this hypothesis remains contentious. Here, we find that differences in the rate and direction of plumage colour evolution are predicted by a proxy for sexual selection intensity (plumage dichromatism) in a large radiation of suboscine passerine birds (Tyrannida). We show that rates of plumage evolution are correlated between the sexes, but that sexual selection has a strong positive effect on male, but not female, interspecific divergence rates. Furthermore, we demonstrate that rapid male plumage divergence is biased towards carotenoid-based (red/yellow) colours widely assumed to represent honest sexual signals. Our results highlight the central role of sexual selection in driving avian colour divergence, and reveal the existence of convergent evolutionary responses of animal signalling traits under sexual selection.

Fig. 1

Sex-specific rate variation in plumage colour evolution across the Tyrannida phylogeny. a, b Plots showing the Tyrannida phylogeny (n = 372 spp.) coloured by estimates of mean relative multivariate rate of plumage colour evolution based on ten body patches for males (a) and females (b). Coloured shapes show the location of significant (posterior probability > 0.99) rate shifts affecting whole clades (triangles) and individual internal branches (circles) (shape colour reflects rate estimate; see Methods for details). Histograms (inset) show the rate distribution for each tree. c Relationship between (log₁₀ transformed) male and female rates of plumage colour evolution (TR_ES values) across species. Phylogenetic reduced major axis regression (solid) and one-to-one (dashed) lines shown. Equation of the regression line: y = 0.10 + 1.15*x (R² = 0.45), which is significantly different to a one-to-one slope (T = 3.69, d.f. = 304.08, P = < 0.001)

Fig. 2

Predictors of rates of plumage colour evolution in the Tyrannida. a Coefficient estimates from a multipredictor BPMM predicting variation in (log₁₀ transformed) whole-plumage TR_ES rates of colour evolution among Tyrannida species (n = 372). Points indicate the mean standardised effect sizes for each of the (scaled) predictor variables and lines indicate 95% credible intervals (CI). Predictors with significant (pMCMC < 0.05) effects are coloured purple (negative effect) and green (positive effect). Marginal R² value (i.e., variance explained by fixed factors) for the full model is 0.23. b Scatterplots showing the relationship between significant predictor variables and plumage rates with regression lines (and 95% CIs) plotted for males (blue) and females (red) separately. Inset values show the change in marginal R² (ΔR²) relative to the full model when a given predictor (and its interaction with sex) is dropped from the full model

Fig. 3

Relationships between dichromatism and rate of plumage colour evolution within body regions for different colouration types. Regression lines are plotted separately for patches consistent with carotenoid-based (orange) or structural (lilac) colouration, as well as colouration intermediate between these two extremes (grey) (see Supplementary Methods). Asterisks indicate whether the slope of the carotenoid regression line (the reference category) is significantly more positive (black) or more negative (red) compared with the slope of the (i) intermediate and (ii) structural regression lines, respectively (i.e., carotenoid slope vs. intermediate slope, carotenoid slope vs. structural slope), based on Bayesian phylogenetic mixed-models. ***pMCMC < 0.001; **pMCMC < 0.01; *pMCMC < 0.05; – non-significant

Fig. 4

The rate and direction of plumage colour divergence among Tyrannida species. Plots combine data from 10 plumage patches for males (a) and females (b) of 372 Tyrannida species. Arrows indicate the direction of evolution and are coloured according to the corresponding patch-specific rate of evolution. Radar plots (inset, a and b) show the mean evolutionary rates of divergence trajectories (black points and lines) falling within each 20^o segment of two-dimensional colour space. Grey bands indicate the 95% confidence intervals for the null distribution of mean rates based on a randomisation process. Filled points indicate values showing significant (P < 0.05) deviations from the null distribution, with triangles and squares indicating faster and slower average rates than expected, respectively. Scale bar (inset, a) and vector diagram showing the loadings of receptor stimulation variables onto PC axes (inset, b) are relevant to both panels