Developmental evolution of sexual ornamentation: model and a test of feather growth and pigmentation.

A tremendous diversity of avian color displays has stimulated numerous studies of natural and sexual selection. Yet, the developmental mechanisms that produce such diversification, and thus the proximate targets of selection pressures, are rarely addressed and poorly understood. In particular, because feathers are colored during growth, the dynamics of feather growth play a deterministic role in the variation in ornamentation. No study to date, however, has addressed the contribution of feather growth to the expression of carotenoid-based ornamentation. Here, we examine the developmental basis of variation in ornamental feather shapes in male house finches (Carpodacus mexicanus)-a species in which carotenoid displays are under strong natural and sexual selection. First, we use geometric morphometrics to partition the observed shape variation in fully grown feathers among populations, ages, degrees of elaboration, ornamental body parts, and individuals. Second, we use a biologically informed mathematical model of feather growth to predict variation in shape of ornamental feathers due to simulated growth rate, angle of helical growth of feather barbs, initial number of barb ridges, rate of addition of new barbs, barb diameter, and ramus-expansion angle. We find close concordance between among-individual variation in feather shape and hue of entire ornament, and show that this concordance can be attributed to a shared mechanism-growth rate of feather barbs. Predicted differences in feather shape due to rate of addition of barbs and helical angle of feather growth explained observed variation in ornamental area both among individuals and between populations, whereas differences in helical angle of growth and the number of barbs in the feather follicle explained differences in feather shape between ornamental parts and among males of different ages. The findings of a close association of feather growth dynamics and overall ornamentation identify the proximate targets of selection for elaboration of sexual displays. Moreover, the close association of feather growth and pigmentation not only can reinforce condition-dependence in color displays, but can also enable phenotypic and genetic accommodation of novel pigments into plumage displays providing a mechanism for the observed concordance of within-population developmental processes and between-population diversification of color displays.