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      Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data

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          Significance

          Ray-finned fishes form the largest and most diverse group of vertebrates. Establishing their phylogenetic relationships is a critical step to explaining their diversity. We compiled the largest comparative genomic database of fishes that provides genome-scale support for previous phylogenetic results and used it to resolve further some contentious relationships in fish phylogeny. A vetted set of exon markers identified in this study is a promising resource for current sequencing approaches to significantly increase genetic and taxonomic coverage to resolve the tree of life for all fishes. Our time-calibrated analysis suggests that most lineages of living fishes were already established in the Mesozoic Period, more than 65 million years ago.

          Abstract

          Our understanding of phylogenetic relationships among bony fishes has been transformed by analysis of a small number of genes, but uncertainty remains around critical nodes. Genome-scale inferences so far have sampled a limited number of taxa and genes. Here we leveraged 144 genomes and 159 transcriptomes to investigate fish evolution with an unparalleled scale of data: >0.5 Mb from 1,105 orthologous exon sequences from 303 species, representing 66 out of 72 ray-finned fish orders. We apply phylogenetic tests designed to trace the effect of whole-genome duplication events on gene trees and find paralogy-free loci using a bioinformatics approach. Genome-wide data support the structure of the fish phylogeny, and hypothesis-testing procedures appropriate for phylogenomic datasets using explicit gene genealogy interrogation settle some long-standing uncertainties, such as the branching order at the base of the teleosts and among early euteleosts, and the sister lineage to the acanthomorph and percomorph radiations. Comprehensive fossil calibrations date the origin of all major fish lineages before the end of the Cretaceous.

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          Most cited references33

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          Is Open Access

          ASTRAL: genome-scale coalescent-based species tree estimation

          Motivation: Species trees provide insight into basic biology, including the mechanisms of evolution and how it modifies biomolecular function and structure, biodiversity and co-evolution between genes and species. Yet, gene trees often differ from species trees, creating challenges to species tree estimation. One of the most frequent causes for conflicting topologies between gene trees and species trees is incomplete lineage sorting (ILS), which is modelled by the multi-species coalescent. While many methods have been developed to estimate species trees from multiple genes, some which have statistical guarantees under the multi-species coalescent model, existing methods are too computationally intensive for use with genome-scale analyses or have been shown to have poor accuracy under some realistic conditions. Results: We present ASTRAL, a fast method for estimating species trees from multiple genes. ASTRAL is statistically consistent, can run on datasets with thousands of genes and has outstanding accuracy—improving on MP-EST and the population tree from BUCKy, two statistically consistent leading coalescent-based methods. ASTRAL is often more accurate than concatenation using maximum likelihood, except when ILS levels are low or there are too few gene trees. Availability and implementation: ASTRAL is available in open source form at https://github.com/smirarab/ASTRAL/. Datasets studied in this article are available at http://www.cs.utexas.edu/users/phylo/datasets/astral. Contact: warnow@illinois.edu Supplementary information: Supplementary data are available at Bioinformatics online.
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            Distinguishing homologous from analogous proteins.

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              Ultraconserved elements anchor thousands of genetic markers spanning multiple evolutionary timescales.

              Although massively parallel sequencing has facilitated large-scale DNA sequencing, comparisons among distantly related species rely upon small portions of the genome that are easily aligned. Methods are needed to efficiently obtain comparable DNA fragments prior to massively parallel sequencing, particularly for biologists working with non-model organisms. We introduce a new class of molecular marker, anchored by ultraconserved genomic elements (UCEs), that universally enable target enrichment and sequencing of thousands of orthologous loci across species separated by hundreds of millions of years of evolution. Our analyses here focus on use of UCE markers in Amniota because UCEs and phylogenetic relationships are well-known in some amniotes. We perform an in silico experiment to demonstrate that sequence flanking 2030 UCEs contains information sufficient to enable unambiguous recovery of the established primate phylogeny. We extend this experiment by performing an in vitro enrichment of 2386 UCE-anchored loci from nine, non-model avian species. We then use alignments of 854 of these loci to unambiguously recover the established evolutionary relationships within and among three ancient bird lineages. Because many organismal lineages have UCEs, this type of genetic marker and the analytical framework we outline can be applied across the tree of life, potentially reshaping our understanding of phylogeny at many taxonomic levels.
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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                12 June 2018
                14 May 2018
                : 115
                : 24
                : 6249-6254
                Affiliations
                [1] aDepartment of Biological Sciences, The George Washington University , Washington, DC 20052;
                [2] bNational Museum of Natural History, Smithsonian Institution , Washington, DC 20560;
                [3] cShenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, Beijing Genomics Institute Academy of Marine Sciences, Beijing Genomics Institute Marine, Beijing Genomics Institute , 518083 Shenzhen, China;
                [4] dBeijing Genomics Institute Education Center, University of Chinese Academy of Sciences , 518083 Shenzhen, China;
                [5] eChina National GeneBank, Beijing Genomics Institute-Shenzhen , 518120 Shenzhen, China;
                [6] fDepartment of Biology, University of Puerto Rico–Rio Piedras , San Juan 00931, Puerto Rico;
                [7] gKey Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University , Ministry of Education, 201306 Shanghai, China;
                [8] hLaboratorio de Ictiología y Acuicultura Experimental, Universidad Nacional del Comahue–CONICET , 8400 Bariloche, Argentina;
                [9] iProfessional Committee of Native Aquatic Organisms and Water Ecosystem, China Fisheries Association , 100125 Beijing, China;
                [10] jCollege of Life Science and Ecology, Hainan Tropical Ocean University , 572022 Sanya, China;
                [11] kYellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences , 266071 Qingdao, China;
                [12] lComparative Genomics Laboratory, Institute of Molecular and Cell Biology, A*STAR , Biopolis, 138673 Singapore
                Author notes

                Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved April 13, 2018 (received for review November 7, 2017)

                Author contributions: L.C.H., G.O., Y.H., Y.S., C.C.B., R.B.-R., B.V., and Q.S. designed research; L.C.H., G.O., Y.H., A.W.T., D.A., R.B.-R., L.B., N.B., X.Z., X.L., M.W., C.F., B.X., and Q.S. performed research; L.C.H., G.O., Y.H., C.C.B., A.W.T., D.A., R.B.-R., Z.Z., H.H., S.C., B.V., and Q.S. contributed new reagents/analytic tools; L.C.H., G.O., Y.H., A.W.T., D.A., R.B.-R., C.L., L.B., N.B., X.Z., X.L., M.W., C.F., and B.X. analyzed data; and L.C.H., G.O., Y.H., D.A., R.B.-R., B.V., and Q.S. wrote the paper.

                1L.C.H., G.O., Y.H., and Y.S. contributed equally to this work.

                Author information
                http://orcid.org/0000-0003-4006-4036
                http://orcid.org/0000-0003-3824-8581
                http://orcid.org/0000-0001-6637-3465
                http://orcid.org/0000-0002-6358-976X
                Article
                PMC6004478 PMC6004478 6004478 201719358
                10.1073/pnas.1719358115
                6004478
                29760103
                9fc52d75-8237-425c-829b-dd938341f0de
                Copyright @ 2018

                Published under the PNAS license.

                History
                Page count
                Pages: 6
                Funding
                Funded by: National Natural Science Foundation of China (NSFC) 501100001809
                Award ID: 31370047
                Funded by: Shenzen Special Program for Strategic Emerging Industries
                Award ID: JSGG20170412153411369
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-147184
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-1541491
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-1457426
                Funded by: National Science Foundation (NSF) 100000001
                Award ID: DEB-1541554
                Categories
                Biological Sciences
                Evolution
                From the Cover

                divergence times,bony fish,phylogenomics,tree of life,paralogy

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