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Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

Molecular Phylogenetics and Evolution, vol. 155, pp. 106967

Abstract

Hybridization can leave genealogical signatures in an organism's genome, originating from the parental lineages and persisting over time. This potentially confounds phylogenetic inference methods that aim to represent evolution as a strictly bifurcating tree. We apply a phylotranscriptomic approach to study the evolutionary history of, and test for inter-lineage introgression in the Salamandridae, a Holarctic salamanders group of interest in studies of toxicity and aposematism, courtship behavior, and molecular evolution. Although the relationships between the 21 currently recognized salamandrid genera have been the subject of numerous molecular phylogenetic studies, some branches have remained controversial and sometimes affected by discordances between mitochondrial vs. nuclear trees. To resolve the phylogeny of this family, and understand the source of mito-nuclear discordance, we generated new transcriptomic (RNAseq) data for 20 salamandrids and used these along with published data, including 28 mitochondrial genomes, to obtain a comprehensive nuclear and mitochondrial perspective on salamandrid evolution. Our final phylotranscriptomic data set included 5455 gene alignments for 40 species representing 17 of the 21 salamandrid genera. Using concatenation and species-tree phylogenetic methods, we find (1) Salamandrina sister to the clade of the "True Salamanders" (consisting of Chioglossa, Mertensiella, Lyciasalamandra, and Salamandra), (2) Ichthyosaura sister to the Near Eastern genera Neurergus and Ommatotriton, (3) Triturus sister to Lissotriton, and (4) Cynops paraphyletic with respect to Paramesotriton and Pachytriton. Combining introgression tests and phylogenetic networks, we find evidence for introgression among taxa within the clades of "Modern Asian Newts" and "Modern European Newts". However, we could not unambiguously identify the number, position, and direction of introgressive events. Combining evidence from nuclear gene analysis with the observed mito-nuclear phylogenetic discordances, we hypothesize a scenario with hybridization and mitochondrial capture among ancestral lineages of (1) Lissotriton into Ichthyosaura and (2) Triturus into Calotriton, plus introgression of nuclear genes from Triturus into Lissotriton. Furthermore, both mitochondrial capture and nuclear introgression may have occurred among lineages assigned to Cynops. More comprehensive genomic data will, in the future, allow testing this against alternative scenarios involving hybridization with other, extinct lineages of newts.

Authors 17

  1. Loïs Rancilhac corresponding

    Technische Universität Braunschweig

    Affiliation as printed

    Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany. Electronic address: loisrancilhac@gmail.com

    Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany

  2. Museo Nacional de Ciencias Naturales

    Affiliation as printed

    Department of Biodiversity and Evolutionary Biology, Museo Nacional de Ciencias Naturales, José Gutiérrez Abascal 2, 28006 Madrid, Spain

  3. Centre de Recherches en Histoire des Idées

    Affiliation as printed

    Via Guglielmo Marconi, 30, 04018 Sezze, Italy

  4. Naturalis Biodiversity Center

    Affiliation as printed

    Naturalis Biodiversity Center, 2300 RA Leiden, the Netherlands

  5. Jagiellonian University

    Affiliation as printed

    Institute of Environmental Sciences, Jagiellonian University, ul. Gronostajowa 7, 30-387 Kraków, Poland

  6. Vrije Universiteit Brussel

    Affiliation as printed

    Amphibian Evolution Lab, Biology Department, Vrije Universiteit Brussel, Pleinlaan 2, B-1050 Brussels Belgium

  7. Max Planck Institute for Evolutionary Biology

    Affiliation as printed

    Max Planck Institute for Evolutionary Biology, 24306 Plön, Germany

  8. LOEWE Centre for Translational Biodiversity Genomics · Fraunhofer Institute for Molecular Biology and Applied Ecology

    Affiliation as printed

    Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Winchesterstr. 2, 35394 Gießen, Germany; LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany

    Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Winchesterstr. 2, 35394 Gießen, Germany

    LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany

  9. Ghent University

    Affiliation as printed

    Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium

  10. Technische Universität Braunschweig · Stanford University

    Affiliation as printed

    Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany; Department of Biology, Stanford University, Stanford, CA 94305, USA

    Department of Biology, Stanford University, Stanford, CA 94305, USA

    Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany

  11. University of Kentucky

    Affiliation as printed

    Department of Biology, University of Kentucky, Lexington, KY 40506, USA

  12. Universität Trier

    Affiliation as printed

    Biogeography Department, Trier University, 54286 Trier, Germany

  13. Leiden University

    Affiliation as printed

    Institute of Biology Leiden, Leiden University, 2300 RA Leiden, the Netherlands

  14. Leipzig University

    Affiliation as printed

    Institute of Biology, Molecular Evolution and Systematics of Animals, University of Leipzig, Talstrasse 33, 04103, Leipzig, Germany

  15. University of Potsdam

    Affiliation as printed

    Faculty of Mathematics and Natural Sciences, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany

  16. Centre National de la Recherche Scientifique · Station d’Écologie Théorique et Expérimentale

    Affiliation as printed

    Centre for Biodiversity Theory and Modelling, UMR CNRS 5321, Station of Theoretical and Experimental Ecology, 2 route du CNRS, 09200 Moulis, France

  17. Technische Universität Braunschweig

    Affiliation as printed

    Zoological Institute, Technische Universität Braunschweig, Mendelssohnstr. 4, 38106 Braunschweig, Germany

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References 101