Morphological Integration Between Developmental Compartments in the Drosophila Wing

Abstract

Abstract. Developmental integration is the covariation among morphological structures due to connections between the developmental processes that built them. Here we use the methods of geometric morphometrics to study integration in the wing of Drosophila melanogaster. In particular, we focus on the hypothesis that the anterior and posterior wing compartments are separate developmental units that vary independently. We measured both variation among genetically diverse individuals and random differences between body sides of single individuals (fluctuating asymmetry, FA). For both of these sources of variation, the patterns of variation identified by principal component analyses all involved landmarks in both the anterior and posterior compartments simultaneously. Analyses focusing exclusively on the covariation between the anterior and posterior compartments, by the partial least‐squares method, revealed pervasive integration of the two compartments, for both individual variation and FA. These analyses clearly indicate that the anterior and posterior compartments are not separate units of variation, but that the covariation between compartments is sufficient to account for nearly all the variation throughout the entire wing. We conclude that variation among individuals as well as the developmental perturbations responsible for FA generate shape variation primarily through developmental processes that are integrated across both compartments. In contrast, much less of the shape variation in our sample can be attributed to the localized processes that establish the identity of particular wing veins.

Studying morphological integration and modularity at multiple levels: concepts and analysis

“…Because fluctuating asymmetry originates from random variation in developmental processes, the asymmetries of different traits are correlated only if there are direct interactions between developmental pathways that produce the traits [46,47]. This approach has been applied in a broad range of animal systems [10,[12][13][14][15]27,36,37,[48][49][50][51][52][53][54][55]. Whereas this reasoning applies widely to motile organisms, including most animals, caution is necessary in applying it to sessile organisms like most plants, where a part of fluctuating asymmetry may be due to plastic responses to heterogeneity in microenvironmental factors [25,56].…”

“…Most empirical studies have focused on integration within populations, investigating how the variation among individuals is structured. This is only one aspect of the problem, however, because the concept of integration also applies at different levels [4], including genetic and environmental integration [8,9], integration of fluctuating asymmetry within individuals [9][10][11][12][13][14][15] and evolutionary integration across taxa in a clade [16][17][18][19][20][21]. Most plants, because of their modular body plans, offer additional opportunities to study integration among structures such as leaves or flowers within and among individuals in a population [22,23].…”

“…Most plants, because of their modular body plans, offer additional opportunities to study integration among structures such as leaves or flowers within and among individuals in a population [22,23]. The distinction of different levels makes it possible to compare patterns of integration between them, in order to gain insight into evolutionary and developmental processes from the resemblance of patterns across the levels of integration [8][9][10][11][12]16,[24][25][26][27].…”

Natural genetic variation in fluctuating asymmetry of wing shape inDrosophila melanogaster

“…Prior to the calculation of FA, we checked for the presence of DA, directional deviations from 180 bilateral symmetry (Klingenberg and Zaklan 2000), and antisymmetry (AS), the two sides are 181 always different but without a predictable direction to the differences. We performed 182…”

Fly wing vein patterns have spatial reproducibility of a single cell

“…Size variations depend on nutritional intake, which is difficult to control experimentally, but at least 75% of wing shape variation is independent of variations in size [21,22], thus allowing us to quantify variations in the final wing vein pattern. To measure variations in the principal pattern features, we apply a succession of affine transformations known as Procrustes transformations on each wing from a given dataset (electronic supplementary material, figure S1) [23,24], which maximally align the wings. The vein pattern for each wing is reduced to the configuration of seven landmark coordinates fx i , y i g, which demarcate wing vein crossing points (figure 1a); wing size is measured by the centroid size S of the configuration (electronic supplementary material, methods and figure S2a).…”