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      Latitudinal clines in gene expression and cis-regulatory element variation in Drosophila melanogaster

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      , ,
      BMC Genomics
      BioMed Central
      Drosophila, Allele-specific expression, Cline

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          Abstract

          Background

          Organisms can rapidly adapt to their environment when colonizing a new habitat, and this could occur by changing protein sequences or by altering patterns of gene expression. The importance of gene expression in driving local adaptation is increasingly being appreciated, and cis-regulatory elements (CREs), which control and modify the expression of the nearby genes, are predicted to play an important role. Here we investigate genetic variation in gene expression in immune-challenged Drosophila melanogaster from temperate and tropical or sub-tropical populations in Australia and United States.

          Results

          We find parallel latitudinal changes in gene expression, with genes involved in immunity, insecticide resistance, reproduction, and the response to the environment being especially likely to differ between latitudes. By measuring allele-specific gene expression (ASE), we show that cis-regulatory variation also shows parallel latitudinal differences between the two continents and contributes to the latitudinal differences in gene expression.

          Conclusions

          Both Australia and United States were relatively recently colonized by D. melanogaster, and it was recently shown that introductions of both African and European flies occurred, with African genotypes contributing disproportionately to tropical populations. Therefore, both the demographic history of the populations and local adaptation may be causing the patterns that we see.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12864-016-3333-7) contains supplementary material, which is available to authorized users.

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          Most cited references32

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Evolution at two levels in humans and chimpanzees.

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              Evolutionary changes in cis and trans gene regulation.

              Differences in gene expression are central to evolution. Such differences can arise from cis-regulatory changes that affect transcription initiation, transcription rate and/or transcript stability in an allele-specific manner, or from trans-regulatory changes that modify the activity or expression of factors that interact with cis-regulatory sequences. Both cis- and trans-regulatory changes contribute to divergent gene expression, but their respective contributions remain largely unknown. Here we examine the distribution of cis- and trans-regulatory changes underlying expression differences between closely related Drosophila species, D. melanogaster and D. simulans, and show functional cis-regulatory differences by comparing the relative abundance of species-specific transcripts in F1 hybrids. Differences in trans-regulatory activity were inferred by comparing the ratio of allelic expression in hybrids with the ratio of gene expression between species. Of 29 genes with interspecific expression differences, 28 had differences in cis-regulation, and these changes were sufficient to explain expression divergence for about half of the genes. Trans-regulatory differences affected 55% (16 of 29) of genes, and were always accompanied by cis-regulatory changes. These data indicate that interspecific expression differences are not caused by select trans-regulatory changes with widespread effects, but rather by many cis-acting changes spread throughout the genome.
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                Author and article information

                Contributors
                fmj1001@cam.ac.uk
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                28 November 2016
                28 November 2016
                2016
                : 17
                : 981
                Affiliations
                Department of Genetics, University of Cambridge, Cambridge, CB2 3EH UK
                Article
                3333
                10.1186/s12864-016-3333-7
                5126864
                27894253
                f6566b6e-9630-40ee-8555-148343d838df
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 4 August 2016
                : 23 November 2016
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: 281668
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2016

                Genetics
                drosophila,allele-specific expression,cline
                Genetics
                drosophila, allele-specific expression, cline

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