Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in <i>Drosophila melanogaster</i>

Levine, Mia T.; Begun, David J.

doi:10.1534/genetics.107.085423

Cited by 24 publications

(26 citation statements)

References 89 publications

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“…These data support the notion that many of the highly differentiated regions identified in the array analysis harbor clinal variation. The analysis presented in the accompanying article (Levine and Begun 2008) also supports the hypothesis that strongly differentiated regions are often clinal.…”

Section: Resultssupporting

confidence: 65%

“…These genes were not significant in Australia, and sequencing verified that they are differentiated only in the United States. Differentiated genes thought to play a role in doublestrand break repair, recombination, or chromosome segregation in Australia include a-tubulin 67C (Matthies et al 1999), egl (Carpenter 1994), tefu (Oikemus et al 2006), and glu (Steffensen et al 2001), with a-tubulin 67C and tefu among the most differentiated loci sequenced (glu sequence data are presented in Levine and Begun 2008). The verified golden probe near spn-D could be related to these functions as well (Abdu et al 2003).…”

Section: Resultsmentioning

confidence: 99%

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Genomic Analysis of Adaptive Differentiation inDrosophila melanogaster

et al. 2008

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Drosophila melanogaster shows clinal variation along latitudinal transects on multiple continents for several phenotypes, allozyme variants, sequence variants, and chromosome inversions. Previous investigation suggests that many such clines are due to spatially varying selection rather than demographic history, but the genomic extent of such selection is unknown. To map differentiation throughout the genome, we hybridized DNA from temperate and subtropical populations to Affymetrix tiling arrays. The dense genomic sampling of variants and low level of linkage disequilibrium in D. melanogaster enabled identification of many small, differentiated regions. Many regions are differentiated in parallel in the United States and Australia, strongly supporting the idea that they are influenced by spatially varying selection. Genomic differentiation is distributed nonrandomly with respect to gene function, even in regions differentiated on only one continent, providing further evidence for the role of selection. These data provide candidate genes for phenotypes known to vary clinally and implicate interesting new processes in genotype-by-environment interactions, including chorion proteins, proteins regulating meiotic recombination and segregation, gustatory and olfactory receptors, and proteins affecting synaptic function and behavior. This portrait of differentiation provides a genomic perspective on adaptation and the maintenance of variation through spatially varying selection.T HE amount and genomic distribution of polymorphism may be influenced by genetic drift, by mutation-selection balance, and by various forms of positive selection such as spatially varying selection, heterozygote advantage, or negative frequency-dependent selection. Spatially varying selection can generate allelefrequency differences between populations in spite of gene flow and lead to local adaptation, which is of particular interest as an intermediate step between intra-and interspecies variation (Felsenstein 1976;Endler 1977;Barton 1983).Drosophila melanogaster has been a model system for investigating the forces maintaining polymorphism for many decades. Indeed, differentiation along latitudinal clines in this species is one of the most thoroughly documented cases of spatially varying selection ( and Singh 1991;Berry and Kreitman 1993;Long and Singh 1995;Gockel et al. 2002;Kennington et al. 2003). The observations that clinal variation is strongly associated with easily measurable phenotypes affecting fitness (Eanes 1999;Gockel et al. 2002;Calboli et al. 2003;Norry et al. 2004;Kennington et al. 2007) and that clines for a number of phenotypes and genetic variants appear to have been independently established on multiple continents (De Jong and Bochdanovits 2003) also strongly support the proposition that many clinal variants are under spatially varying selection and that the biology of temperate and tropical populations may be quite different.Nevertheless, these data represent a small and highly biased picture of the phenotypes and...

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Section: Resultssupporting

confidence: 65%

Section: Resultsmentioning

confidence: 99%

Genomic Analysis of Adaptive Differentiation inDrosophila melanogaster

et al. 2008

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“…More recent studies focused only on selection stabilizing the temperature-sensitive transcriptional output by directly acting on the proteins of the PcG system in populations from temperate environments (Harr et al 2002;Levine and Begun 2008;Gibert et al 2011). In this study, we present evidence for selection acting on cis-regulatory sequences to reduce the temperature sensitivity of PcG-regulated gene expression.…”

Section: Discussionmentioning

confidence: 71%

“…PcG-regulated genes are temperature sensitive in their expression; i.e., their transcriptional output is higher when flies are reared or held at lower temperatures than at higher ones (Fauvarque and Dura 1993;Chan et al 1994;Zink and Paro 1995;Bantignies et al 2003;Gibert et al 2011). This phenomenon prompted the hypothesis that if cold temperatures disrupt PcG regulation, then adaptation to temperate environments should include the buffering of this expression plasticity (Levine and Begun 2008). Natural selection would then act to stabilize the transcriptional output, leading to a lower degree of gene expression plasticity in response to varying temperatures.…”

Section: Discussionmentioning

confidence: 99%

“…Several recent studies (Harr et al 2002;Levine and Begun 2008;Gibert et al 2011) explored the question of whether the temperature-induced expression plasticity of PcG-regulated genes may have been detrimental to D. melanogaster while settling in temperate environments. These studies suggest that adaptation included selection acting to buffer this thermosensitive process in temperate populations.…”

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Positive Selection at thePolyhomeoticLocus Led to Decreased Thermosensitivity of Gene Expression in TemperateDrosophila melanogaster

Voigt¹,

Laurent²,

Litovchenko³

et al. 2015

Genetics

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Drosophila melanogaster as a cosmopolitan species has successfully adapted to a wide range of different environments. Variation in temperature is one important environmental factor that influences the distribution of species in nature. In particular for insects, which are mostly ectotherms, ambient temperature plays a major role in their ability to colonize new habitats. Chromatinbased gene regulation is known to be sensitive to temperature. Ambient temperature leads to changes in the activation of genes regulated in this manner. One such regulatory system is the Polycomb group (PcG) whose target genes are more expressed at lower temperatures than at higher ones. Therefore, a greater range in ambient temperature in temperate environments may lead to greater variability (plasticity) in the expression of these genes. This might have detrimental effects, such that positive selection acts to lower the degree of the expression plasticity. We provide evidence for this process in a genomic region that harbors two PcG-regulated genes, polyhomeotic proximal (ph-p) and CG3835. We found a signature of positive selection in this gene region in European populations of D. melanogaster and investigated the region by means of reporter gene assays. The target of selection is located in the intergenic fragment between the two genes. It overlaps with the promoters of both genes and an experimentally validated Polycomb response element (PRE). This fragment harbors five sequence variants that are highly differentiated between European and African populations. The African alleles confer a temperature-induced plasticity in gene expression, which is typical for PcG-mediated gene regulation, whereas thermosensitivity is reduced for the European alleles.

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A survey of the trans-regulatory landscape for Drosophila melanogaster abdominal pigmentation

Rogers

Grover

Stringer

et al. 2014

Developmental Biology

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Trait development results from the collaboration of genes interconnected in hierarchical networks that control which genes are activated during the progression of development. While networks are understood to change over developmental time, the alterations that occur over evolutionary times are much less clear. A multitude of transcription factors and a far greater number of linkages between transcription factors and cis-regulatory elements (CREs) have been found to structure well-characterized networks, but the best understood networks control traits that are deeply conserved. Fruit fly abdominal pigmentation may represent an optimal setting to study network evolution, as this trait diversified over short evolutionary time spans. However, the current understanding of the underlying network includes a small set of transcription factor genes. Here, we greatly expand this network through an RNAi-screen of 558 transcription factors. We identified 28 genes, including previously implicated abd-A, Abd-B, bab1, bab2, dsx, exd, hth, and jing, as well as 20 novel factors with uncharacterized roles in pigmentation development. These include genes which promote pigmentation, suppress pigmentation, and some that have either male- or female-limited effects. We show that many of these transcription factors control the reciprocal expression of two key pigmentation enzymes, whereas a subset controls the expression of key factors in a female-specific circuit. We found the pupal Abd-A expression pattern was conserved between species with divergent pigmentation, indicating diversity resulted from changes to other loci. Collectively, these results reveal a greater complexity of the pigmentation network, presenting numerous opportunities to map transcription factor-CRE interactions that structure trait development and numerous candidate loci to investigate as potential targets of evolution.

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Evidence of Spatially Varying Selection Acting on Four Chromatin-Remodeling Loci in Drosophila melanogaster

Cited by 24 publications

References 89 publications

Genomic Analysis of Adaptive Differentiation inDrosophila melanogaster

Genomic Analysis of Adaptive Differentiation inDrosophila melanogaster

Positive Selection at thePolyhomeoticLocus Led to Decreased Thermosensitivity of Gene Expression in TemperateDrosophila melanogaster

A survey of the trans-regulatory landscape for Drosophila melanogaster abdominal pigmentation

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