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      The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict

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          Abstract

          The evolutionary relationships among the apicomplexan blood pathogens known as the malaria parasites (order Haemosporida), some of which infect nearly 200 million humans each year, has remained a vexing phylogenetic problem due to limitations in taxon sampling, character sampling and the extreme nucleotide base composition biases that are characteristic of this clade. Previous phylogenetic work on the malaria parasites has often lacked sufficient representation of the broad taxonomic diversity within the Haemosporida or the multi-locus sequence data needed to resolve deep evolutionary relationships, rendering our understanding of haemosporidian life-history evolution and the origin of the human malaria parasites incomplete. Here we present the most comprehensive phylogenetic analysis of the malaria parasites conducted to date, using samples from a broad diversity of vertebrate hosts that includes numerous enigmatic and poorly known haemosporidian lineages in addition to genome-wide multi-locus sequence data. We find that if base composition differences were corrected for during phylogenetic analysis, we recovered a well-supported topology indicating that the evolutionary history of the malaria parasites was characterized by a complex series of transitions in life-history strategies and host usage. Notably we find that Plasmodium, the malaria parasite genus that includes the species of human medical concern, is polyphyletic with the life-history traits characteristic of this genus having evolved in a dynamic manner across the phylogeny. We find support for multiple instances of gain and loss of asexual proliferation in host blood cells and production of haemozoin pigment, two traits that have been used for taxonomic classification as well as considered to be important factors for parasite virulence and used as drug targets. Lastly, our analysis illustrates the need for a widespread reassessment of malaria parasite taxonomy.

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          TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations

          We present TranslatorX, a web server designed to align protein-coding nucleotide sequences based on their corresponding amino acid translations. Many comparisons between biological sequences (nucleic acids and proteins) involve the construction of multiple alignments. Alignments represent a statement regarding the homology between individual nucleotides or amino acids within homologous genes. As protein-coding DNA sequences evolve as triplets of nucleotides (codons) and it is known that sequence similarity degrades more rapidly at the DNA than at the amino acid level, alignments are generally more accurate when based on amino acids than on their corresponding nucleotides. TranslatorX novelties include: (i) use of all documented genetic codes and the possibility of assigning different genetic codes for each sequence; (ii) a battery of different multiple alignment programs; (iii) translation of ambiguous codons when possible; (iv) an innovative criterion to clean nucleotide alignments with GBlocks based on protein information; and (v) a rich output, including Jalview-powered graphical visualization of the alignments, codon-based alignments coloured according to the corresponding amino acids, measures of compositional bias and first, second and third codon position specific alignments. The TranslatorX server is freely available at http://translatorx.co.uk.
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            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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              The 'effective number of codons' used in a gene.

              F. Wright (1990)
              A simple measure is presented that quantifies how far the codon usage of a gene departs from equal usage of synonymous codons. This measure of synonymous codon usage bias, the 'effective number of codons used in a gene', Nc, can be easily calculated from codon usage data alone, and is independent of gene length and amino acid (aa) composition. Nc can take values from 20, in the case of extreme bias where one codon is exclusively used for each aa, to 61 when the use of alternative synonymous codons is equally likely. Nc thus provides an intuitively meaningful measure of the extent of codon preference in a gene. Codon usage patterns across genes can be investigated by the Nc-plot: a plot of Nc vs. G + C content at synonymous sites. Nc-plots are produced for Homo sapiens, Saccharomyces cerevisiae, Escherichia coli, Bacillus subtilis, Dictyostelium discoideum, and Drosophila melanogaster. A FORTRAN77 program written to calculate Nc is available on request.
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                Author and article information

                Journal
                R Soc Open Sci
                R Soc Open Sci
                RSOS
                royopensci
                Royal Society Open Science
                The Royal Society Publishing
                2054-5703
                May 2018
                23 May 2018
                23 May 2018
                : 5
                : 5
                : 171780
                Affiliations
                [1 ]Sackler Institute for Comparative Genomics, American Museum of Natural History , Central Park West at 79th St., New York, NY 10024, USA
                [2 ]Richard Gilder Graduate School, American Museum of Natural History , Central Park West at 79th St., New York, NY 10024, USA
                [3 ]Institute of Zoology, Biocenter Grindel, University of Hamburg , Martin-Luther-King-Platz 3, D-20146 Hamburg, Germany
                [4 ]Center for Conservation Genomics, Smithsonian Conservation Biology Institute , National Zoological Park, PO Box 37012, MRC5503, Washington, DC 20013-7012, USA
                [5 ]Department of Biology, Humboldt University , 10115, Berlin, Germany
                [6 ]Department of Biological Sciences, Museum of Natural Science, Louisiana State University , Baton Rouge, LA 70803, USA
                [7 ]Wildlife Program, Yurok Tribe , Klamath, CA 95548, USA
                Author notes
                Authors for correspondence: Spencer C. Galen e-mail: spgalen@ 123456gmail.com
                Authors for correspondence: Susan L. Perkins e-mail: perkins@ 123456amnh.org

                Electronic supplementary material is available online at https://dx.doi.org/10.6084/m9.figshare.c.4091723.

                Author information
                http://orcid.org/0000-0003-0209-1535
                Article
                rsos171780
                10.1098/rsos.171780
                5990803
                29892372
                23ef8959-9fdf-455c-b847-fde03142dce9
                © 2018 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : 1 November 2017
                : 20 April 2018
                Funding
                Funded by: Division of Environmental Biology, http://dx.doi.org/10.13039/100000155;
                Award ID: 1145984
                Award ID: 1146033
                Categories
                1001
                70
                183
                197
                Biology (Whole Organism)
                Research Article
                Custom metadata
                May, 2018

                plasmodium,malaria,phylogeny,base composition bias,polyphyly

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