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      Rapid evolution of the intersexual genetic correlation for fitness in Drosophila melanogaster

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          Abstract

          Sexual antagonism (SA) arises when male and female phenotypes are under opposing selection, yet genetically correlated. Until resolved, antagonism limits evolution toward optimal sex‐specific phenotypes. Despite its importance for sex‐specific adaptation and existing theory, the dynamics of SA resolution are not well understood empirically. Here, we present data from Drosophila melanogaster, compatible with a resolution of SA. We compared two independent replicates of the “LH M” population in which SA had previously been described. Both had been maintained under identical, controlled conditions, and separated for around 200 generations. Although heritabilities of male and female fitness were similar, the intersexual genetic correlation differed significantly, being negative in one replicate (indicating SA) but close to zero in the other. Using population sequencing, we show that phenotypic differences were associated with population divergence in allele frequencies at nonrandom loci across the genome. Large frequency changes were more prevalent in the population without SA and were enriched at loci mapping to genes previously shown to have sexually antagonistic relationships between expression and fitness. Our data suggest that rapid evolution toward SA resolution has occurred in one of the populations and open avenues toward studying the genetics of SA and its resolution.

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          Using FlyAtlas to identify better Drosophila melanogaster models of human disease.

          FlyAtlas, a new online resource, provides the most comprehensive view yet of expression in multiple tissues of Drosophila melanogaster. Meta-analysis of the data shows that a significant fraction of the genome is expressed with great tissue specificity in the adult, demonstrating the need for the functional genomic community to embrace a wide range of functional phenotypes. Well-known developmental genes are often reused in surprising tissues in the adult, suggesting new functions. The homologs of many human genetic disease loci show selective expression in the Drosophila tissues analogous to the affected human tissues, providing a useful filter for potential candidate genes. Additionally, the contributions of each tissue to the whole-fly array signal can be calculated, demonstrating the limitations of whole-organism approaches to functional genomics and allowing modeling of a simple tissue fractionation procedure that should improve detection of weak or tissue-specific signals.
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            Is Open Access

            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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              Intralocus sexual conflict.

              Intralocus sexual conflict occurs when selection on a shared trait in one sex displaces the other sex from its phenotypic optimum. It arises because many shared traits have a common genetic basis but undergo contrasting selection in the sexes. A recent surge of interest in this evolutionary tug of war has yielded evidence of such conflicts in laboratory and natural populations. Here we highlight outstanding questions about the causes and consequences of intralocus sexual conflict at the genomic level, and its long-term implications for sexual coevolution. Whereas recent thinking has focussed on the role of intralocus sexual conflict as a brake on sexual coevolution, we urge a broader appraisal that also takes account of its potential to drive adaptive evolution and speciation.
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                Author and article information

                Contributors
                m.reuter@ucl.ac.uk
                Journal
                Evolution
                Evolution
                10.1111/(ISSN)1558-5646
                EVO
                Evolution; International Journal of Organic Evolution
                John Wiley and Sons Inc. (Hoboken )
                0014-3820
                1558-5646
                17 March 2016
                April 2016
                : 70
                : 4 ( doiID: 10.1111/evo.2016.70.issue-4 )
                : 781-795
                Affiliations
                [ 1 ] Research Department of Genetics, Evolution and EnvironmentUniversity College London LondonUnited Kingdom
                [ 2 ] Current Address: School of Biological SciencesUniversity of Queensland St. Lucia QLDAustralia
                [ 3 ] Department of Animal EcologyUppsala University UppsalaSweden
                [ 4 ] Current Address: School of Life SciencesUniversity of Sussex BrightonUnited Kingdom
                Author notes
                [†]

                These authors contributed equally to this work.

                Article
                EVO12892
                10.1111/evo.12892
                5069644
                27077679
                df4bf90c-9a2f-4221-ac28-20b1fd9fad38
                © 2016 The Author(s). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 23 November 2014
                : 16 February 2016
                : 17 February 2016
                Page count
                Pages: 15
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                evo12892
                April 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.5 mode:remove_FC converted:19.10.2016

                Evolutionary Biology
                adaptation,evolutionary genomics,fitness,population genetics,quantitative genetics,sexual conflict

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