Behavior evolves as a correlated response to selection on cuticle color in Drosophila melanogaster and D. simulans

Abstract

To predict adaptive evolution, we need to understand the degree to which selection on one trait can constrain or redirect evolutionary responses in other traits. We used artificial selection on cuticle color in Drosophila melanogaster and D. simulans to investigate whether color and behavior evolve in tandem. We selected for light and dark thoracic colors for 16 generations in two populations per species and measured correlated responses in aggression, basal activity, total activity, sleep, and geotaxis. Dark selected individuals consistently showed higher aggression and basal activity than light selected or control flies across both species and sexes, pointing to a modest but repeatable correlated response. In contrast, patterns for geotaxis, sleep, and total activity evolved unpredictably, often varying across species and populations, and showed no clear association with color. Within-population phenotypic correlations between color and aggression were significant but weak (rho = -0.035, rho{superscript 2} = 0.001), suggesting that color is a poor predictor of individual aggressive behavior. Populations evolving higher aggression also tended to evolve higher basal activity (rho = 0.52, p = 0.004), suggesting activity may have evolved as a correlated response rather than through a direct color-activity link. The persistence of correlated responses in aggression and basal activity in response to selection on color is consistent with a conserved genetic basis, such as pleiotropy or linkage disequilibrium, although our data do not distinguish between these mechanisms. Identifying the loci underlying variation in both color and behavior, and testing their effects experimentally, will clarify how multivariate genetic covariance shapes the direction and pace of adaptive evolution.