Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

Loïs Rancilhac, Iker Irisarri, Claudio Angelini, Jan W. Arntzen, Wiesław Babik, Franky Bossuyt, Sven Künzel, Tim Lüddecke, Frank Pasmans, Eugenia Sanchez, David Weisrock, Michael Veith, Ben Wielstra, Sebastian Steinfartz, Michael Hofreiter, Hervé Philippe, Miguel Vences

Research output: Contribution to journalArticlepeer-review

18 Scopus citations

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.

Original languageEnglish
Article number106967
JournalMolecular Phylogenetics and Evolution
Volume155
DOIs
StatePublished - Feb 2021

Bibliographical note

Funding Information:
We are grateful to Uwe Seidel for help with obtaining samples and to Paul Hime for generating the Cynops cyanurus data. LR, MH and MVen were supported by the Deutsche Forschungsgemeinschaft (grant VE247/16-1 – HO 3492/6-1) in the framework of the “TaxonOmics” priority program. II was supported by a Juan de la Cierva–Incorporación postdoctoral fellowship (IJCI-2016- 29566) from the Spanish Ministry of Economy and Competitiviness (MINECO). ES was supported by the Deutscher Akademischer Austauschdienst (DAAD).

Publisher Copyright:
© 2020 Elsevier Inc.

Keywords

  • Amphibia
  • Introgression
  • Phylogenetic network
  • Phylogenomics
  • RNAseq
  • Salamandridae

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

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