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.

Plastic flies

“…13 To muddy the waters further, wing size is more developmentally stable, and shows lower levels of fluctuating asymmetry, than genital size. 13 The ambiguity of our data concerning the existence of a universal buffering mechanism reflects the wider literature, with some studies supporting the hypothesis 9,11,14 and others rejecting it. 7,8,15 These studies (ours included) are essentially correlative, comparing and contrasting variability in different traits in response to different environmental and genetic perturbations.…”

“…4 An ongoing question in the study of variability is whether the same buffering mechanisms that regulate genetic variability also regulate environmental variability and developmental instability. [7][8][9][10][11] Data from our laboratory is equivocal on this issue. We have shown that environmental variability in trait size in Drosophila depends on the source of environmental variation.…”

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].…”

“…A simple measure of the resemblance between covariance matrices is matrix correlation, the correlation between corresponding entries in two covariance matrices. Matrix correlations have long been used in analyses of morphological integration using traditional morphometrics [8] and have been adapted for use in geometric morphometrics [9,11,13,25,53]. For instance, a multilevel analysis of integration in the leaves of cinquefoil plants found that the patterns of static integration within species and of evolutionary integration were remarkably similar, whereas the pattern of fluctuating asymmetry was more distinct [25].…”

Symmetry is beauty – or is it?

“…L'étude de la modularité développementale et de son impact sur l'évolution est un sujet de recherche majeur de « l'évo-dévo » (à l'infterface de l'évolution et du développement) [40]. Enfin, quelques études ont tenté d'explorer explicitement les bases génétiques et développementales de l'asymétrie fluctuante, soit par des cribles génétiques [41,42], soit par l'étude détaillée de gènes candidats [7,43]. La question fondamentale est de savoir s'il existe un (ou des) système(s) génétique(s) dont la fonction première serait d'assurer la stabilité du déve-loppement ou, au contraire, si les structures en déve-loppement sont intrinsèquement robustes aux perturbations.…”