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      Eight Million Years of Satellite DNA Evolution in Grasshoppers of the Genus Schistocerca Illuminate the Ins and Outs of the Library Hypothesis

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          Abstract

          Satellite DNA (satDNA) is an abundant class of tandemly repeated noncoding sequences, showing high rate of change in sequence, abundance, and physical location. However, the mechanisms promoting these changes are still controversial. The library model was put forward to explain the conservation of some satDNAs for long periods, predicting that related species share a common collection of satDNAs, which mostly experience quantitative changes. Here, we tested the library model by analyzing three satDNAs in ten species of Schistocerca grasshoppers. This group represents a valuable material because it diversified during the last 7.9 Myr across the American continent from the African desert locust ( Schistocerca gregaria), and this thus illuminates the direction of evolutionary changes. By combining bioinformatic and cytogenetic, we tested whether these three satDNA families found in S. gregaria are also present in nine American species, and whether differential gains and/or losses have occurred in the lineages. We found that the three satDNAs are present in all species but display remarkable interspecies differences in their abundance and sequences while being highly consistent with genus phylogeny. The number of chromosomal loci where satDNA is present was also consistent with phylogeny for two satDNA families but not for the other. Our results suggest eminently chance events for satDNA evolution. Several evolutionary trends clearly imply either massive amplifications or contractions, thus closely fitting the library model prediction that changes are mostly quantitative. Finally, we found that satDNA amplifications or contractions may influence the evolution of monomer consensus sequences and by chance playing a major role in driftlike dynamics.

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          The evolutionary dynamics of repetitive DNA in eukaryotes.

          Repetitive DNA sequences form a large portion of the genomes of eukaryotes. The 'selfish DNA' hypothesis proposes that they are maintained by their ability to replicate within the genome. The behaviour of repetitive sequences can result in mutations that cause genetic diseases, and confer significant fitness losses on the organism. Features of the organization of repetitive sequences in eukaryotic genomes, and their distribution in natural populations, reflect the evolutionary forces acting on selfish DNA.
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            RepeatExplorer: a Galaxy-based web server for genome-wide characterization of eukaryotic repetitive elements from next-generation sequence reads.

            Repetitive DNA makes up large portions of plant and animal nuclear genomes, yet it remains the least-characterized genome component in most species studied so far. Although the recent availability of high-throughput sequencing data provides necessary resources for in-depth investigation of genomic repeats, its utility is hampered by the lack of specialized bioinformatics tools and appropriate computational resources that would enable large-scale repeat analysis to be run by biologically oriented researchers. Here we present RepeatExplorer, a collection of software tools for characterization of repetitive elements, which is accessible via web interface. A key component of the server is the computational pipeline using a graph-based sequence clustering algorithm to facilitate de novo repeat identification without the need for reference databases of known elements. Because the algorithm uses short sequences randomly sampled from the genome as input, it is ideal for analyzing next-generation sequence reads. Additional tools are provided to aid in classification of identified repeats, investigate phylogenetic relationships of retroelements and perform comparative analysis of repeat composition between multiple species. The server allows to analyze several million sequence reads, which typically results in identification of most high and medium copy repeats in higher plant genomes.
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              Molecular drive: a cohesive mode of species evolution.

              G. Dover (1982)
              It is generally accepted that mutations may become fixed in a population by natural selection and genetic drift. In the case of many families of genes and noncoding sequences, however, fixation of mutations within a population may proceed as a consequence of molecular mechanisms of turnover within the genome. These mechanisms can be both random and directional in activity. There are circumstances in which the unusual concerted pattern of fixation permits the establishment of biological novelty and species discontinuities in a manner not predicted by the classical genetics of natural selection and genetic drift.
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                Author and article information

                Contributors
                Role: Associate Editor
                Journal
                Genome Biol Evol
                Genome Biol Evol
                gbe
                Genome Biology and Evolution
                Oxford University Press
                1759-6653
                March 2020
                17 March 2020
                17 March 2020
                : 12
                : 3
                : 88-102
                Affiliations
                [e1 ] Department of Evolutionary Biology, Evolutionary Biology Centre, Uppsala University , Sweden
                [e2 ] Departamento de Biologia Geral e Aplicada, Instituto de Biociências/IB, UNESP – Univ Estadual Paulista , Rio Claro, São Paulo, Brazil
                [e3 ] Department of Entomology, Texas A&M University
                [e4 ] Laboratorio de Genética Evolutiva, IBS, Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones , CONICET, Posadas, Argentina
                [e5 ] Departamento de Genética, Facultad de Ciencias , UGR – Univ de Granada, Spain
                [e6 ] Department of Organismal Biology, Systematic Biology, Evolutionary Biology Centre, Uppsala University , Uppsala, Sweden
                Author notes
                Author information
                http://orcid.org/0000-0002-1472-9949
                Article
                evaa018
                10.1093/gbe/evaa018
                7093836
                32211863
                0311b43c-ca35-4264-916f-1888a04392fd
                © The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 30 January 2020
                Page count
                Pages: 15
                Funding
                Funded by: Fundação de Amparo à Pesquisa do Estado de São Paulo-FAPESP;
                Award ID: 2014/11763-8
                Funded by: Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior-CAPES;
                Funded by: U.S. National Science Foundation;
                Award ID: IOS-1253493
                Funded by: United State Department of Agriculture;
                Funded by: Consejo Nacional de Investigaciones Científicas y Técnicas-CONICET from Argentina;
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico-CNPq;
                Award ID: 304758/2014-0
                Categories
                Research Article

                Genetics
                chromosomal evolution,genome organization,tandem repeats,repetitive dna
                Genetics
                chromosomal evolution, genome organization, tandem repeats, repetitive dna

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