Differences in the selection response of serially repeated color pattern characters: Standing variation, development, and evolution

Abstract

BackgroundThere is spectacular morphological diversity in nature but lineages typically display a limited range of phenotypes. Because developmental processes generate the phenotypic variation that fuels natural selection, they are a likely source of evolutionary biases, facilitating some changes and limiting others. Although shifts in developmental regulation are associated with morphological differences between taxa, it is unclear how underlying mechanisms affect the rate and direction of evolutionary change within populations under selection.Here we focus on two ecologically relevant features of butterfly wing color patterns, eyespot size and color composition, which are similarly and strongly correlated across the serially repeated eyespots. Though these two characters show similar patterns of standing variation and covariation within a population, they differ in key features of their underlying development. We targeted pairs of eyespots with artificial selection for coordinated (concerted selection) versus independent (antagonistic selection) change in their color composition and size and compared evolutionary responses of the two color pattern characters.ResultsThe two characters respond to selection in strikingly different ways despite initially similar patterns of variation in all directions present in the starting population. Size (determined by local properties of a diffusing inductive signal) evolves flexibly in all selected directions. However, color composition (determined by a tissue-level response to the signal concentration gradient) evolves only in the direction of coordinated change. There was no independent evolutionary change in the color composition of two eyespots in response to antagonistic selection. Moreover, these differences in the directions of short-term evolutionary change in eyespot size and color composition within a single species are consistent with the observed wing pattern diversity in the genus.ConclusionBoth characters respond rapidly to selection for coordinated change, but there are striking differences in their response to selection for antagonistic, independent change across eyespots. While many additional factors may contribute to both short- and long-term evolutionary response, we argue that the compartmentalization of developmental processes can influence the diversification of serial repeats such as butterfly eyespots, even under strong selection.

Evolution of adaptive phenotypic variation patterns by direct selection for evolvability

“…The idea that selection could directly act on evolvability is controversial [39], but in recent years computational models have shown that selection for evolvability is probably a generic property of all but the most simplistic genetic models ([40-45]; see also [46] for an empirical example). The present model, together with the demonstration of the existence of quasi-'neutral' rQTL variation [17,23,24], shows that selection may be able to modify the genetic architecture to increase evolvability and, specifically, increase the response rate to directional selection.…”

Evolution of Drosophila sex comb length illustrates the inextricable interplay between selection and variation

“…For image acquisition, adult legs were dissected, and mounted on cover slips 22X22 mm No 1 (VWR), viewed with an Olympus BX41M and imaged with a Cool Snap camera U-CMAD (Photometrics) following protocols previously described (12,24). Angles were measured using the angle tool of Image J software (http://rsb.info.nih.gov/ij).…”

“…For example, artificial selection in the butterfly, Bicyclus anynana, have shown that the size of eyespots and wings displays a rapid and pronounced response (10,11). In contrast, a developmental constraint has been inferred when selection fails to uncouple traits as in the failure to robustly uncouple changes in the diameter of the black and gold eyespot rings in B. anynana (8,12). Although comparative studies have proposed a compelling list of potential developmental constraints, there is little experimental evidence demonstrating mechanisms underlying their existence (5,6,9).…”

Morphological Evolution Repeatedly Caused by Mutations in Signaling Ligand Genes

“…Indeed, the variation involves little differences in pattern shape or number and instead consists in color composition differences. A difference in signal sensitivity rather than signal strength between the two forms is more likely to explain the phenomenon, resulting in a threshold trait variation (see Allen et al 2008 for a discussion of pattern size vs. color composition). We thus predict that this polymorphism could map to a Wnt-pathway gene or to a gene that can modify the output of the Wnt signaling pathway and that this gene should be active during the extracellular signaling phase or shortly thereafter.…”