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      Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies.

      1 , 2 , 3 , 4 , 2 , 5 , 6 , 7 , 8 , 9 , 2 , 10 , 8 , 2 , 2 , 2 , 11 , 12 , 13 , 14 , 8 , 15 , 16 , 2 , 17 , 18
      Proceedings of the National Academy of Sciences of the United States of America
      Proceedings of the National Academy of Sciences
      DNA methylation, genome sequencing, phenotypic plasticity, social evolution, transcriptomes

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          Abstract

          Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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          Most cited references58

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          Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise.

          A major goal of biology is to provide a quantitative description of cellular behaviour. This task, however, has been hampered by the difficulty in measuring protein abundances and their variation. Here we present a strategy that pairs high-throughput flow cytometry and a library of GFP-tagged yeast strains to monitor rapidly and precisely protein levels at single-cell resolution. Bulk protein abundance measurements of >2,500 proteins in rich and minimal media provide a detailed view of the cellular response to these conditions, and capture many changes not observed by DNA microarray analyses. Our single-cell data argue that noise in protein expression is dominated by the stochastic production/destruction of messenger RNAs. Beyond this global trend, there are dramatic protein-specific differences in noise that are strongly correlated with a protein's mode of transcription and its function. For example, proteins that respond to environmental changes are noisy whereas those involved in protein synthesis are quiet. Thus, these studies reveal a remarkable structure to biological noise and suggest that protein noise levels have been selected to reflect the costs and potential benefits of this variation.
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            Phenotypic plasticity's impacts on diversification and speciation.

            Phenotypic plasticity (the ability of a single genotype to produce multiple phenotypes in response to variation in the environment) is commonplace. Yet its evolutionary significance remains controversial, especially in regard to whether and how it impacts diversification and speciation. Here, we review recent theory on how plasticity promotes: (i) the origin of novel phenotypes, (ii) divergence among populations and species, (iii) the formation of new species and (iv) adaptive radiation. We also discuss the latest empirical support for each of these evolutionary pathways to diversification and identify potentially profitable areas for future research. Generally, phenotypic plasticity can play a largely underappreciated role in driving diversification and speciation. Copyright (c) 2010 Elsevier Ltd. All rights reserved.
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              The genetic causes of convergent evolution.

              The evolution of phenotypic similarities between species, known as convergence, illustrates that populations can respond predictably to ecological challenges. Convergence often results from similar genetic changes, which can emerge in two ways: the evolution of similar or identical mutations in independent lineages, which is termed parallel evolution; and the evolution in independent lineages of alleles that are shared among populations, which I call collateral genetic evolution. Evidence for parallel and collateral evolution has been found in many taxa, and an emerging hypothesis is that they result from the fact that mutations in some genetic targets minimize pleiotropic effects while simultaneously maximizing adaptation. If this proves correct, then the molecular changes underlying adaptation might be more predictable than has been appreciated previously.
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                Author and article information

                Journal
                Proc. Natl. Acad. Sci. U.S.A.
                Proceedings of the National Academy of Sciences of the United States of America
                Proceedings of the National Academy of Sciences
                1091-6490
                0027-8424
                Nov 10 2015
                : 112
                : 45
                Affiliations
                [1 ] The Babraham Institute, Cambridge CB22 3AT, United Kingdom; solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
                [2 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain;
                [3 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom;
                [4 ] The Babraham Institute, Cambridge CB22 3AT, United Kingdom; Department of Biochemistry and Biophysics, Science for Life Laboratory, Stockholm University, Stockholm 106 91, Sweden;
                [5 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Instituto de Investigação e Inovação em Saúde, Universidade do Porto, 4200-135 Porto, Portugal; Institute of Molecular Pathology and Immunology of the University of Porto (IPATIMUP), Institute of Molecular Pathology and Immunology, University of Porto, 4200-135 Porto, Portugal;
                [6 ] Institute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom; Institute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom;
                [7 ] Institute of Biochemistry, University of Stuttgart, 70569 Stuttgart, Germany;
                [8 ] The Babraham Institute, Cambridge CB22 3AT, United Kingdom;
                [9 ] Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom; Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom;
                [10 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Max Planck Institute for Molecular Genetics, 14195 Berlin, Germany;
                [11 ] Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto (FFCLRP)-Universidade de São Paulo, 14040-901, Ribeirão Preto-SP, Brazil;
                [12 ] Department of Chemistry, University of Cambridge, Cambridge CB2 1EW, United Kingdom; Cancer Research UK Cambridge Institute, University of Cambridge, Cambridge CB2 ORE, United Kingdom; School of Clinical Medicine, University of Cambridge, CB2 0SP, Cambridge, United Kingdom;
                [13 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Institució Catalana de Recerca i Estudis Avançats, 08010 Barcelona, Spain;
                [14 ] School of Earth Sciences, University of Bristol, BS8 1TQ, United Kingdom;
                [15 ] Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003 Barcelona, Spain; Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain; Department of Biotechnology, Universität für Bodenkultur, 1190 Vienna, Austria;
                [16 ] Institute of Integrative and Comparative Biology, School of Biology, University of Leeds, Leeds LS2 9JT, United Kingdom; School of Life Sciences, University of Sussex, Brighton BN1 9QG, United Kingdom;
                [17 ] The Babraham Institute, Cambridge CB22 3AT, United Kingdom; Centre for Trophoblast Research, University of Cambridge, Cambridge CB2 3EG, United Kingdom; Wellcome Trust Sanger Institute, Hinxton CB10 1SA, United Kingdom solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
                [18 ] School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom; Institute of Zoology, Zoological Society of London, London NW1 4RY, United Kingdom; solenn.patalano@babraham.ac.uk wolf.reik@babraham.ac.uk seirian.sumner@bristol.ac.uk.
                Article
                1515937112
                10.1073/pnas.1515937112
                4653166
                26483466
                cff6b576-780c-4c56-a391-460e4e47cf59
                History

                DNA methylation,genome sequencing,phenotypic plasticity,social evolution,transcriptomes

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