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      Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster

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          Abstract

          Insect cuticular hydrocarbons (CHCs) prevent desiccation and serve as chemical signals that mediate social interactions. Drosophila melanogaster CHCs have been studied extensively, but the genetic basis for individual variation in CHC composition is largely unknown. We quantified variation in CHC profiles in the D. melanogaster Genetic Reference Panel (DGRP) and identified novel CHCs. We used principal component (PC) analysis to extract PCs that explain the majority of CHC variation and identified polymorphisms in or near 305 and 173 genes in females and males, respectively, associated with variation in these PCs. In addition, 17 DGRP lines contain the functional Desat2 allele characteristic of African and Caribbean D. melanogaster females (more 5,9-C27:2 and less 7,11-C27:2, female sex pheromone isomers). Disruption of expression of 24 candidate genes affected CHC composition in at least one sex. These genes are associated with fatty acid metabolism and represent mechanistic targets for individual variation in CHC composition.

          DOI: http://dx.doi.org/10.7554/eLife.09861.001

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          The outermost layer of an insect’s body is called the epicuticle and is made of a blend of fat molecules. “Cuticular hydrocarbons” (or CHCs) are the most common fat molecules in the epicuticle, and play an important role in protecting the insect’s body from harsh, dry habitats. CHCs also have other roles in insect behavior. For example, these molecules act as chemical cues when insects search for mates (i.e. pheromones), and they can even contribute to camouflage.

          Insects are amongst the most diverse groups of animals on Earth, and different species have different blends of CHC molecules in their epicuticles. Fruit flies are a useful model to understand the genetics of CHC production, including CHCs that act as sex pheromones. Previous research has analyzed the CHCs made by both sexes in several fruit fly strains. However this work was unable to uncover which genes influence how much of a given CHC an individual fly will make.

          Dembeck et al. have now looked into CHC production in a collection of 205 different fly strains, all of which have already had their total genetic material sequenced and studied. Comparing these known sequences and looking for associations between genetic differences and particular CHCs uncovered 24 genes that may be involved in CHC manufacture. Only six of the genes had been identified previously. Dembeck et al. found that interfering with the activity of any of the 24 genes had a knock-on effect on many other CHCs present in the flies’ epicuticle.

          These 24 genes could to be pieced together in a network that is needed to make and recycle CHCs. The complexity and flexibility of this network can explain in part how insects have been able to build epicuticles for almost every environment. These data set the stage for future work directed towards understanding the evolutionary significance of variation in CHC composition in many fruit fly populations.

          DOI: http://dx.doi.org/10.7554/eLife.09861.002

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          Most cited references51

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          Natural variation in genome architecture among 205 Drosophila melanogaster Genetic Reference Panel lines

          The Drosophila melanogaster Genetic Reference Panel (DGRP) is a community resource of 205 sequenced inbred lines, derived to improve our understanding of the effects of naturally occurring genetic variation on molecular and organismal phenotypes. We used an integrated genotyping strategy to identify 4,853,802 single nucleotide polymorphisms (SNPs) and 1,296,080 non-SNP variants. Our molecular population genomic analyses show higher deletion than insertion mutation rates and stronger purifying selection on deletions. Weaker selection on insertions than deletions is consistent with our observed distribution of genome size determined by flow cytometry, which is skewed toward larger genomes. Insertion/deletion and single nucleotide polymorphisms are positively correlated with each other and with local recombination, suggesting that their nonrandom distributions are due to hitchhiking and background selection. Our cytogenetic analysis identified 16 polymorphic inversions in the DGRP. Common inverted and standard karyotypes are genetically divergent and account for most of the variation in relatedness among the DGRP lines. Intriguingly, variation in genome size and many quantitative traits are significantly associated with inversions. Approximately 50% of the DGRP lines are infected with Wolbachia , and four lines have germline insertions of Wolbachia sequences, but effects of Wolbachia infection on quantitative traits are rarely significant. The DGRP complements ongoing efforts to functionally annotate the Drosophila genome. Indeed, 15% of all D. melanogaster genes segregate for potentially damaged proteins in the DGRP, and genome-wide analyses of quantitative traits identify novel candidate genes. The DGRP lines, sequence data, genotypes, quality scores, phenotypes, and analysis and visualization tools are publicly available.
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            A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac.

            With the availability of complete genome sequence for Drosophila melanogaster, one of the next strategic goals for fly researchers is a complete gene knockout collection. The P-element transposon, the workhorse of D. melanogaster molecular genetics, has a pronounced nonrandom insertion spectrum. It has been estimated that 87% saturation of the approximately 13,500-gene complement of D. melanogaster might require generating and analyzing up to 150,000 insertions. We describe specific improvements to the lepidopteran transposon piggyBac and the P element that enabled us to tag and disrupt genes in D. melanogaster more efficiently. We generated over 29,000 inserts resulting in 53% gene saturation and a more diverse collection of phenotypically stronger insertional alleles. We found that piggyBac has distinct global and local gene-tagging behavior from that of P elements. Notably, piggyBac excisions from the germ line are nearly always precise, piggyBac does not share chromosomal hotspots associated with P and piggyBac is more effective at gene disruption because it lacks the P bias for insertion in 5' regulatory sequences.
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              Ecological, behavioral, and biochemical aspects of insect hydrocarbons.

              This review covers selected literature from 1982 to the present on some of the ecological, behavioral, and biochemical aspects of hydrocarbon use by insects and other arthropods. Major ecological and behavioral topics are species- and gender-recognition, nestmate recognition, task-specific cues, dominance and fertility cues, chemical mimicry, and primer pheromones. Major biochemical topics include chain length regulation, mechanism of hydrocarbon formation, timing of hydrocarbon synthesis and transport, and biosynthesis of volatile hydrocarbon pheromones of Lepidoptera and Coleoptera. In addition, a section is devoted to future research needs in this rapidly growing area of science.
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                Author and article information

                Contributors
                Role: Reviewing editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                14 November 2015
                2015
                : 4
                : e09861
                Affiliations
                [1 ]deptDepartment of Biological Sciences , North Carolina State University , Raleigh, United States
                [2 ]deptGenetics Program , North Carolina State University , Raleigh, United States
                [3 ]deptW. M. Keck Center for Behavioral Biology , North Carolina State University , Raleigh, United States
                [4 ]deptDepartment of Entomology , North Carolina State University , Raleigh, United States
                [5]University of California, Davis , United States
                [6]University of California, Davis , United States
                Author notes
                [†]

                Ecology and Evolution Unit, Okinawa Institute of Science and Technology, Onna-son, Japan.

                [‡]

                Department of Neurobiology and Behavior and Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, United States.

                Article
                09861
                10.7554/eLife.09861
                4749392
                26568309
                46a0fce5-824e-4e37-a597-eeb6a415b695
                © 2015, Dembeck et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 03 July 2015
                : 12 November 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01 GM59469
                Award Recipient :
                Funded by: Blanton J Whitmore Endowment;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01 GM45146
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Genomics and Evolutionary Biology
                Custom metadata
                2.5
                Genome wide association analyses in a wild-derived Drosophila melanogaster population uncover extensive variation in cuticular hydrocarbon composition, which may present a target for natural selection and adaptive evolution.

                Life sciences
                genome wide associaiton study,drosophila genetic reference panel,cuticular lipids,african drosophila,multivariate analysis,d. melanogaster

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