Developmental constraints in the Drosophila wing

Guerra, Daniela; Pezzoli, Maria Cristina; Giorgi, Gianfranco; Garoia, Flavio; Cavicchi, Sandro

doi:10.1038/hdy.1997.200

Cited by 37 publications

(29 citation statements)

References 15 publications

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“…Selection favoring specific character combinations can build or contribute to phenotypic and genetic covariation [30,36,37,82] via linkage disequilibrium. This type of covariation is expected to break down rapidly under antagonistic selection [83], and the breakdown of linkage disequilibrium created by past natural selection on eyespot size (for combinations of overall larger or smaller eyespots) may have contributed to the rapid independent evolution of eyespot sizes under antagonistic selection [57].…”

Section: Resultsmentioning

confidence: 99%

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

et al. 2008

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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.

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Section: Resultsmentioning

confidence: 99%

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

et al. 2008

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“…1). Mostly analyzing distances among landmarks defined on the wing, Cavicchi et al (1981Cavicchi et al ( , 1985 have suggested that these compartments are evolutionarily independent (see also Guerra et al 1997;). However, a recent geometric morphometric study focusing on the effect of both genetic and random developmental variations on wing shape (Klingenberg and Zaklan 2000) has provided arguments against this view and concluded that shape changes should be considered as fundamentally integrated across the entire wing.…”

Section: Integration Versus Modularitymentioning

confidence: 98%

“…The emphasis of analyses of Drosophila wing development has recently shifted from integration to modularity (Klingenberg and Zaklan 2000). This shift is based on both developmental and evolutionary genetic studies that have suggested that the wing is composed of genetically independent developmental modules (e.g., Garcia-Bellido et al 1973, see below;Cavicchi et al 1981Cavicchi et al , 1985Guerra et al 1997;Birdsall et al 2000;Zimmerman et al 2000;Weber et al 2001). However, a recent study devoted to the analysis of the patterns of integration in the Drosophila wing (Klingenberg and Zaklan 2000) showed that both genetic variance and fluctuating asymmetry simultaneously affect the entire wing, leading the authors to suggest that Drosophila wing should be viewed as fundamentally integrated rather than modular.…”

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confidence: 96%

Allometric and Nonallometric Components of Drosophila Wing Shape Respond Differently to Developmental Temperature

Debat¹,

Bégin²,

Legout³

et al. 2003

Evol

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“…They concluded that the compartments are distinct units because of differences in amount or direction of the response to selection (Cavicchi et al 1981(Cavicchi et al , 1985(Cavicchi et al , 1991Guerra et al 1997) or different degrees of geographic variation (Imasheva et al 1995;Pezzoli et al 1997). Most of these studies were based on measurements of several distances between landmarks, areas of intervein regions, or measures of cell size and number in different regions of the wing.…”

Section: Covariation Of Anterior and Posterior Compartmentsmentioning

confidence: 99%

“…The subdivision of fly wings into anterior and posterior compartments ( Fig. Accordingly, a number of studies have used morphometric approaches to examine whether anterior and posterior wing compartments are distinct as modules that are reflected in phenotypic and genetic variation (Cavicchi et al 1981(Cavicchi et al , 1985(Cavicchi et al , 1991Thompson and Woodruff 1982;Cowley and Atchley 1990;Guerra et al 1997;Pezzoli et al 1997;Baylac and Penin 1998). Accordingly, a number of studies have used morphometric approaches to examine whether anterior and posterior wing compartments are distinct as modules that are reflected in phenotypic and genetic variation (Cavicchi et al 1981(Cavicchi et al , 1985(Cavicchi et al , 1991Thompson and Woodruff 1982;Cowley and Atchley 1990;Guerra et al 1997;Pezzoli et al 1997;Baylac and Penin 1998).…”

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confidence: 99%

Morphological Integration Between Developmental Compartments in the Drosophila Wing

Klingenberg

Zaklan

2000

Evol

118

158

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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.

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Developmental constraints in the Drosophila wing

Cited by 37 publications

References 15 publications

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

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

Allometric and Nonallometric Components of Drosophila Wing Shape Respond Differently to Developmental Temperature

Morphological Integration Between Developmental Compartments in the Drosophila Wing

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