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      Ancient horizontal transfers of retrotransposons between birds and ancestors of human pathogenic nematodes

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          Abstract

          Parasite host switches may trigger disease emergence, but prehistoric host ranges are often unknowable. Lymphatic filariasis and loiasis are major human diseases caused by the insect-borne filarial nematodes Brugia, Wuchereria and Loa. Here we show that the genomes of these nematodes and seven tropical bird lineages exclusively share a novel retrotransposon, AviRTE, resulting from horizontal transfer (HT). AviRTE subfamilies exhibit 83–99% nucleotide identity between genomes, and their phylogenetic distribution, paleobiogeography and invasion times suggest that HTs involved filarial nematodes. The HTs between bird and nematode genomes took place in two pantropical waves, >25–22 million years ago (Myr ago) involving the Brugia/ Wuchereria lineage and >20–17 Myr ago involving the Loa lineage. Contrary to the expectation from the mammal-dominated host range of filarial nematodes, we hypothesize that these major human pathogens may have independently evolved from bird endoparasites that formerly infected the global breadth of avian biodiversity.

          Abstract

          Lymphatic filariasis and loiasis are diseases caused by insect-borne filarial nematodes. Here, Suh et al. identify a retrotransposon that is present in the genomes of these nematodes and seven tropical bird lineages, indicating two waves of horizontal gene transfer around 17–25 million years ago.

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          Most cited references38

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          Horizontal gene transfer in eukaryotic evolution.

          Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.
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            RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography.

            We announce the release of Reconstruct Ancestral State in Phylogenies (RASP), a user-friendly software package for inferring historical biogeography through reconstructing ancestral geographic distributions on phylogenetic trees. RASP utilizes the widely used Statistical-Dispersal Vicariance Analysis (S-DIVA), the Dispersal-Extinction-Cladogenesis (DEC) model (Lagrange), a Statistical DEC model (S-DEC) and BayArea. It provides a graphical user interface (GUI) to specify a phylogenetic tree or set of trees and geographic distribution constraints, draws pie charts on the nodes of a phylogenetic tree to indicate levels of uncertainty, and generates high-quality exportable graphical results. RASP can run on both Windows and Mac OS X platforms. All documentation and source code for RASP is freely available at http://mnh.scu.edu.cn/soft/blog/RASP.
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              Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes.

              Although common among bacteria, lateral gene transfer-the movement of genes between distantly related organisms-is thought to occur only rarely between bacteria and multicellular eukaryotes. However, the presence of endosymbionts, such as Wolbachia pipientis, within some eukaryotic germlines may facilitate bacterial gene transfers to eukaryotic host genomes. We therefore examined host genomes for evidence of gene transfer events from Wolbachia bacteria to their hosts. We found and confirmed transfers into the genomes of four insect and four nematode species that range from nearly the entire Wolbachia genome (>1 megabase) to short (<500 base pairs) insertions. Potential Wolbachia-to-host transfers were also detected computationally in three additional sequenced insect genomes. We also show that some of these inserted Wolbachia genes are transcribed within eukaryotic cells lacking endosymbionts. Therefore, heritable lateral gene transfer occurs into eukaryotic hosts from their prokaryote symbionts, potentially providing a mechanism for acquisition of new genes and functions.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                21 April 2016
                2016
                : 7
                : 11396
                Affiliations
                [1 ]Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University , SE-752 36 Uppsala, Sweden
                [2 ]Department of Biology and Museum of Southwestern Biology, University of New Mexico , Albuquerque, New Mexico 87131, USA
                [3 ]Department of Conservation Biology, Helmholtz Centre for Environmental Research (UFZ) , D-04318 Leipzig, Germany
                [4 ]Molecular Evolution and Systematics of Animals, Institute of Biology, University of Leipzig , D-04103 Leipzig, Germany
                [5 ]Instituto Nacional de Pesquisas da Amazônia (INPA) , AM 69067-375 Manaus, Brazil
                [6 ]Department of Biological Sciences, National University of Singapore , Singapore 117543, Singapore
                [7 ]Institute of Evolutionary Biology and Ecology, University of Bonn , D-53121 Bonn, Germany
                [8 ]Max Planck Institute for Evolutionary Anthropology , D-04103 Leipzig, Germany
                [9 ]Museum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley , Berkeley, California 94720, USA
                [10 ]National Center for Genome Resources , Santa Fe, New Mexico 87505, USA
                [11 ]Department of Organismic and Evolutionary Biology, Harvard University , Cambridge, Massachusetts 02138, USA
                Author notes
                [*]

                Present address: Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK

                Article
                ncomms11396
                10.1038/ncomms11396
                4844689
                27097561
                1d87a9fe-0442-48d1-92ce-4418968eab9c
                Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 21 July 2015
                : 21 March 2016
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