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      Accumulation of Deleterious Mutations in Landlocked Threespine Stickleback Populations

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          Abstract

          Colonization of new habitats often reduces population sizes and may result in the accumulation of deleterious mutations by genetic drift. Compared with the genomic basis for adaptation to new environments, genome-wide analysis of deleterious mutations in isolated populations remains limited. In the present study, we investigated the accumulation of deleterious mutations in five endangered freshwater populations of threespine stickleback ( Gasterosteus aculeatus) in the central part of the mainland of Japan. Using whole-genome resequencing data, we first conducted phylogenomic analysis and confirmed at least two independent freshwater colonization events in the central mainland from ancestral marine ecotypes. Next, analyses of single nucleotide polymorphisms showed a substantial reduction of heterozygosity in freshwater populations compared with marine populations. Reduction in heterozygosity was more apparent at the center of each chromosome than the peripheries and on X chromosomes compared with autosomes. Third, bioinformatic analysis of deleterious mutations showed increased accumulation of putatively deleterious mutations in the landlocked freshwater populations compared with marine populations. For the majority of populations examined, the frequencies of putatively deleterious mutations were higher on X chromosomes than on autosomes. The interpopulation comparison indicated that the majority of putatively deleterious mutations may have accumulated independently. Thus, whole-genome resequencing of endangered populations can help to estimate the accumulation of deleterious mutations and inform us of which populations are the most severely endangered. Furthermore, analysis of variation among chromosomes can give insights into whether any particular chromosomes are likely to accumulate deleterious mutations.

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          Most cited references72

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          The genomic basis of adaptive evolution in threespine sticklebacks

          Summary Marine stickleback fish have colonized and adapted to innumerable streams and lakes formed since the last ice age, providing an exceptional opportunity to characterize genomic mechanisms underlying repeated ecological adaptation in nature. Here we develop a high quality reference genome assembly for threespine sticklebacks. By sequencing the genomes of 20 additional individuals from a global set of marine and freshwater populations, we identify a genome-wide set of loci that are consistently associated with marine-freshwater divergence. Our results suggest that reuse of globally-shared standing genetic variation, including chromosomal inversions, plays an important role in repeated evolution of distinct marine and freshwater sticklebacks, and in the maintenance of divergent ecotypes during early stages of reproductive isolation. Both coding and regulatory changes occur in the set of loci underlying marine-freshwater evolution, with regulatory changes likely predominating in this classic example of repeated adaptive evolution in nature.
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            Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.

            Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.
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              The hitch-hiking effect of a favourable gene.

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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
                April 2020
                07 April 2020
                07 April 2020
                : 12
                : 4
                : 479-492
                Affiliations
                [e1 ] Ecological Genetics Laboratory, National Institute of Genetics , Mishima, Shizuoka, Japan
                [e2 ] Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo , Norway
                [e3 ] Graduate School of Life Sciences, Tohoku University , Sendai, Miyagi, Japan
                [e4 ] Comparative Genomics Laboratory, National Institute of Genetics , Mishima, Shizuoka, Japan
                [e5 ] Department of Marine Bioscience, Fukui Prefectural University , Obama, Fukui, Japan
                [e6 ] Biological Laboratories, Gifu-kyoritsu University , Ogaki, Gifu, Japan
                [e7 ] Max Planck Institute for Developmental Biology , Tübingen, Germany
                [e8 ] School of Life Sciences, University of Nottingham, University Park , Nottingham, United Kingdom
                Author notes
                Corresponding author: E-mail: jkitano@ 123456nig.ac.jp .
                Author information
                http://orcid.org/0000-0003-4600-9353
                Article
                evaa065
                10.1093/gbe/evaa065
                7197494
                32232440
                757c7913-9ca9-40d2-9944-ac571ee518d4
                © 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 Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 24 March 2020
                Page count
                Pages: 14
                Categories
                Research Article

                Genetics
                hariyo,mutation load,provean,sift,sex chromosome,nonsynonymous
                Genetics
                hariyo, mutation load, provean, sift, sex chromosome, nonsynonymous

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