Microarray Analysis of Replicate Populations Selected Against a Wing-Shape Correlation in Drosophila melanogaster

Department of Biological Sciences, University of Southern Maine, Portland, Maine 04104-9300, USA.
Genetics (Impact Factor: 5.96). 03/2008; 178(2):1093-108. DOI: 10.1534/genetics.107.078014
Source: PubMed


We selected bidirectionally to change the phenotypic correlation between two wing dimensions in Drosophila melanogaster and measured gene expression differences in late third instar wing disks, using microarrays. We tested an array of 12 selected lines, including 10 from a Massachusetts population (5 divergently selected pairs) and 2 from a California population (1 divergently selected pair). In the Massachusetts replicates, 29 loci showed consistent, significant expression differences in all 5 line-pair comparisons. However, the significant loci in the California lines were almost completely different from these. The disparity between responding genes in different gene pools confirms recent evidence that surprisingly large numbers of loci can affect wing shape. Our results also show that with well-replicated selection lines, of large effective size, the numbers of candidate genes in microarray-based searches can be reduced to realistic levels.

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    • "However, these studies were performed using adult flies whereas studies of expression patterns of specific tissues (e.g. wing imaginal discs in third instar wandering larvae) have not discriminated between sexes [30,44,45]. Therefore, it would be very helpful for future investigations to analyze the expression patterns of wing imaginal discs in males and females separately. "
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    ABSTRACT: The Drosophila wing represents a particularly appropriate model to investigate the developmental control of phenotypic variation. Previous studies which aimed to identify candidate genes for wing morphology demonstrated that the genetic basis of wing shape variation in D. melanogaster is composed of numerous genetic factors causing small, additive effects. In this study, we analyzed wing shape in males and females from 191 lines of D. melanogaster, homozygous for a single P-element insertion, using geometric morphometrics techniques. The analysis allowed us to identify known and novel candidate genes that may contribute to the expression of wing shape in each sex separately and to compare them to candidate genes affecting wing size which have been identified previously using the same lines. Our results indicate that more than 63% of induced mutations affected wing shape in one or both sexes, although only 33% showed significant differences in both males and females. The joint analysis of wing size and shape revealed that only 19% of the P-element insertions caused coincident effects on both components of wing form in one or both sexes. Further morphometrical analyses revealed that the intersection between veins showed the smallest displacements in the proximal region of the wing. Finally, we observed that mutations causing general deformations were more common than expected in both sexes whereas the opposite occurred with those generating local changes. For most of the 94 candidate genes identified, this seems to be the first record relating them with wing shape variation. Our results support the idea that the genetic architecture of wing shape is complex with many different genes contributing to the trait in a sexually dimorphic manner. This polygenic basis, which is relatively independent from that of wing size, is composed of genes generally involved in development and/or metabolic functions, especially related to the regulation of different cellular processes such as motility, adhesion, communication and signal transduction. This study suggests that understanding the genetic basis of wing shape requires merging the regulation of vein patterning by signalling pathways with processes that occur during wing development at the cellular level.
    Full-text · Article · Jun 2011 · BMC Developmental Biology
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    • "These are often members of conserved growth regulation pathways such as cell cycle, insulin signaling and apoptosis (Hafen and Stocker 2003). Studies of quantitative wing shape variation within D. melanogaster have implicated several of these genes as potential contributors to intraspecific variation (Dworkin and Gibson 2006, Weber et al 2008). Wing shape across the Drosophila genus is remarkably conserved (Houle et al. 2003) and may be under stabilizing selection or canalization (Gilchrist et al. 2000). "
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    ABSTRACT: How do morphological differences between species evolve at the genetic level? This study investigates the genetic basis of recent divergence in male wing size between species of the model parasitoid wasp Nasonia. The forewings of flightless Nasonia vitripennis males are 2.3 times smaller than males of their flighted sister species N. giraulti. We describe a major genetic contributor to this difference: the sex-specific widerwing (wdw) locus, which we have backcrossed from N. giraulti into N. vitripennis and mapped to an 0.9 megabase region of chromosome 1. This introgression of wdw from large-winged N. giraulti into small-winged N. vitripennis increases male but not female forewing width by 30% through wing region-specific size changes. Indirect evidence suggests that cell number changes across the wing explain the majority of the wdw wing-size difference, whereas changes in cell size are important in the center of the wing. Introgressing the same locus from the other species in the genus, N. longicornis and N. oneida, into N. vitripennis produces intermediate and large male wing sizes. To our knowledge, this is the first study to introgress a morphological quantitative trait locus (QTL) from multiple species into a common genetic background. Epistatic interactions between wdw and other QTL are also identified by introgressing wdw from N. vitripennis into N. giraulti. The main findings are (1) the changes at wdw have sex- and region-specific effects and could, therefore, be regulatory, (2) the wdw locus seems to be a co-regulator of cell size and cell number, and (3) the wdw locus has evolved different wing width effects in three species.
    Full-text · Article · Mar 2010 · Heredity
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    • "), the two divergent lines were mixed and allowed to interbreed for 34 generations, at which time they were reselected for the same wing para meter divergence—four replicates in each direction—for another 25 generations (Weber et al. 2008). "
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    ABSTRACT: Recent results from a variety of different kinds of experiments, mainly using behavior as an assay, and ranging from laboratory selection experiments to gene interaction studies, show that a much wider range of genes can affect phenotype than those identified as "core genes" in classical mutant screens. Moreover, very pleiotropic genes can produce specific phenotypes when mild variants are combined. These studies also show that gene networks readily change configuration and the relationships between interacting genes in response to the introduction of additional genetic variants, suggesting that the networks range widely and have a high degree of flexibility and malleability. Such flexibility, in turn, offers a plausible mechanism for the molding of phenotypes through microevolution, as a prerequisite to making a suitable environment for the acceptance of newly arising large-effect mutations in the transition from microevolution to macroevolution.
    Preview · Article · Nov 2009 · Cold Spring Harbor Symposia on Quantitative Biology
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