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

A tremendous diversity of avian color displays has stimulatednumerous studies of natural and sexual selection. Yet, the developmentalmechanisms that produce such diversification, and thus the proximatetargets of selection pressures, are rarely addressed and poorlyunderstood. In particular, because feathers are colored duringgrowth, the dynamics of feather growth play a deterministicrole in the variation in ornamentation. No study to date, however,has addressed the contribution of feather growth to the expressionof carotenoid-based ornamentation. Here, we examine the developmentalbasis of variation in ornamental feather shapes in male housefinches (Carpodacus mexicanus)—a species in which carotenoiddisplays are under strong natural and sexual selection. First,we use geometric morphometrics to partition the observed shapevariation in fully grown feathers among populations, ages, degreesof elaboration, ornamental body parts, and individuals. Second,we use a biologically informed mathematical model of feathergrowth to predict variation in shape of ornamental feathersdue to simulated growth rate, angle of helical growth of featherbarbs, initial number of barb ridges, rate of addition of newbarbs, barb diameter, and ramus-expansion angle. We find closeconcordance between among-individual variation in feather shapeand hue of entire ornament, and show that this concordance canbe attributed to a shared mechanism—growth rate of featherbarbs. Predicted differences in feather shape due to rate ofaddition of barbs and helical angle of feather growth explainedobserved variation in ornamental area both among individualsand between populations, whereas differences in helical angleof growth and the number of barbs in the feather follicle explaineddifferences in feather shape between ornamental parts and amongmales of different ages. The findings of a close associationof feather growth dynamics and overall ornamentation identifythe proximate targets of selection for elaboration of sexualdisplays. Moreover, the close association of feather growthand pigmentation not only can reinforce condition-dependencein color displays, but can also enable phenotypic and geneticaccommodation of novel pigments into plumage displays providinga mechanism for the observed concordance of within-populationdevelopmental processes and between-population diversificationof color displays.