A single basis for developmental buffering of Drosophila wing shape

Abstract

The nature of developmental buffering processes has been debated extensively, based on both theoretical reasoning and empirical studies. In particular, controversy has focused on the question of whether distinct processes are responsible for canalization, the buffering against environmental or genetic variation, and for developmental stability, the buffering against random variation intrinsic in developmental processes. Here, we address this question for the size and shape of Drosophila melanogaster wings in an experimental design with extensively replicated and fully controlled genotypes. The amounts of variation among individuals and of fluctuating asymmetry differ markedly among genotypes, demonstrating a clear genetic basis for size and shape variability. For wing shape, there is a high correlation between the amounts of variation among individuals and fluctuating asymmetry, which indicates a correspondence between the two types of buffering. Likewise, the multivariate patterns of shape variation among individuals and of fluctuating asymmetry show a close association. For wing size, however, the amounts of individual variation and fluctuating asymmetry are not correlated. There was a significant link between the amounts of variation between wing size and shape, more so for fluctuating asymmetry than for variation among individuals. Overall, these experiments indicate a considerable degree of shared control of individual variation and fluctuating asymmetry, although it appears to differ between traits.

Figure 1. The set of 15 landmarks used in this study.

Figure 2. Relationships between individual variation and FA for shape and size.

(A) Shape variation and FA quantified by Procrustes distance. (B) Shape variation and FA quantified using Mahalanobis distance. (C) Variation and FA of centroid size. The solid lines are major axis regression lines, and the dashed lines in (A) and (C) are the theoretical limits for the situation when left and right sides are independent (FA variance is 4 times the variance among individuals; see text for details).

Figure 3. Relationships between size and shape for FA (A, B) and for individual variation (C, D).

Figure 4. Matrix correlations between the covariance matrices for individual variation and FA.

(A) Matrix correlations including the diagonal blocks (variances and covariances for x and y coordinates of each landmark). (B) Matrix correlations for covariance matrices without the diagonal blocks (only covariances among landmarks).