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      The genomic substrate for adaptive radiation in African cichlid fish

      research-article
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          Abstract

          Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia ( Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.

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          Most cited references36

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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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            Insights into hominid evolution from the gorilla genome sequence

            Summary Gorillas are humans’ closest living relatives after chimpanzees, and are of comparable importance for the study of human origins and evolution. Here we present the assembly and analysis of a genome sequence for the western lowland gorilla, and compare the whole genomes of all extant great ape genera. We propose a synthesis of genetic and fossil evidence consistent with placing the human-chimpanzee and human-chimpanzee-gorilla speciation events at approximately 6 and 10 million years ago (Mya). In 30% of the genome, gorilla is closer to human or chimpanzee than the latter are to each other; this is rarer around coding genes, indicating pervasive selection throughout great ape evolution, and has functional consequences in gene expression. A comparison of protein coding genes reveals approximately 500 genes showing accelerated evolution on each of the gorilla, human and chimpanzee lineages, and evidence for parallel acceleration, particularly of genes involved in hearing. We also compare the western and eastern gorilla species, estimating an average sequence divergence time 1.75 million years ago, but with evidence for more recent genetic exchange and a population bottleneck in the eastern species. The use of the genome sequence in these and future analyses will promote a deeper understanding of great ape biology and evolution.
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              Evolution of microRNA diversity and regulation in animals.

              In the past decade, microRNAs (miRNAs) have been uncovered as key regulators of gene expression at the post-transcriptional level. The ancient origin of miRNAs, their dramatic expansion in bilaterian animals and their function in providing robustness to transcriptional programmes suggest that miRNAs are instrumental in the evolution of organismal complexity. Advances in understanding miRNA biology, combined with the increasing availability of diverse sequenced genomes, have begun to reveal the molecular mechanisms that underlie the evolution of miRNAs and their targets. Insights are also emerging into how the evolution of miRNA-containing regulatory networks has contributed to organismal complexity.
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                Author and article information

                Journal
                0410462
                6011
                Nature
                Nature
                Nature
                0028-0836
                1476-4687
                26 February 2015
                03 September 2014
                18 September 2014
                18 March 2015
                : 513
                : 7518
                : 375-381
                Affiliations
                [1 ]Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA.
                [2 ]MRC Functional Genomics Unit, University of Oxford, Oxford OX1 3QX, UK.
                [3 ]Department of Fish Ecology and Evolution, Eawag Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution & Biogeochemistry, CH-6047 Kastanienbaum, Switzerland.
                [4 ]Division of Aquatic Ecology, Institute of Ecology & Evolution, University of Bern, CH-3012 Bern, Switzerland.
                [5 ]Gurdon Institute, Cambridge CB2 1QN, UK.
                [6 ]Wellcome Trust Sanger Institute, Hinxton CB10 1SA, UK.
                [7 ]Department of Biology, University of Konstanz, D-78457 Konstanz, Germany.
                [8 ]European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
                [9 ]Institute of Molecular and Cell Biology, A*STAR, 138673 Singapore.
                [10 ]Department of Biology, Reed College, Portland, Oregon 97202, USA.
                [11 ]Biology Department, Stanford University, Stanford, California 94305-5020, USA.
                [12 ]Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, California 91125, USA.
                [13 ]Benaroya Research Institute at Virginia Mason, Seattle, Washington 98101, USA.
                [14 ]Institut Génétique et Développement, CNRS/University of Rennes, 35043 Rennes, France.
                [15 ]CIRAD, Campus International de Baillarguet, TA B-110/A, 34398 Montpellier cedex 5, France.
                [16 ]School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332-0230, USA.
                [17 ]Department of Biology, University of Maryland, College Park, Maryland 20742, USA.
                [18 ]Animal Genetics, Institute of Animal Science, ARO, The Volcani Center, Bet-Dagan, 50250 Israel.
                [19 ]Zoological Institute, University of Basel, CH-4051 Basel, Switzerland.
                [20 ]Department of Integrative Biology, Center for Computational Biology and Bioinformatics; The University of Texas at Austin, Austin, Texas 78712, USA.
                [21 ]Department of Biological Sciences, Tokyo Institute of Technology, Tokyo, 226-8501 Yokohama, Japan.
                [22 ]Systématique, Adaptation, Evolution, National Museum of Natural History, 75005 Paris, France.
                [23 ]Institute of Aquaculture, University of Stirling, Stirling FK9 4LA, UK.
                [24 ]Carnegie Institution of Washington, Department of Embryology, 3520 San Martin Drive Baltimore, Maryland 21218, USA.
                [25 ]National Cheng Kung University, Tainan City, 704 Taiwan.
                [26 ]Science for Life Laboratory, Department of Medical Biochemistry and Microbiology, Uppsala University, 751 23 Uppsala, Sweden.
                [27 ]Vertebrate and Health Genomics, The Genome Analysis Centre, Norwich NR18 7UH, UK.
                Author notes
                Correspondence and requests for materials should be addressed to F.D.P. ( Federica.di-palma@ 123456tgac.ac.uk ), K.L.-T. ( Kersli@ 123456broadinstitute.org ), J.T.S. ( todd.streelman@ 123456biology.gatech.edu ), and O.S. ( ole.seehausen@ 123456eawag.ch ).
                Article
                NIHMS656279
                10.1038/nature13726
                4353498
                25186727
                2bcd9683-2fdc-4665-9174-3fe19d6274d3
                ©2014 Macmillan Publishers Limited. All rights reserved

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