Phylotranscriptomic evidence for pervasive ancient hybridization among Old World salamanders

[Display omitted] •We present the first family-wide phylogenomic dataset for the Salamandridae.•Transcriptomic and mitochondrial analyses recover a new position for Salamandrina.•Transcriptomic data confirm mito-nuclear discordances in several groups of newts.•Ancient introgressive hybridization lik...

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Published in:	Molecular phylogenetics and evolution 2021-02, Vol.155, p.106967, Article 106967
Main Authors:	Rancilhac, Loïs, Irisarri, Iker, Angelini, Claudio, Arntzen, Jan W., Babik, Wiesław, Bossuyt, Franky, Künzel, Sven, Lüddecke, Tim, Pasmans, Frank, Sanchez, Eugenia, Weisrock, David, Veith, Michael, Wielstra, Ben, Steinfartz, Sebastian, Hofreiter, Michael, Philippe, Hervé, Vences, Miguel
Format:	Article
Language:	eng
Subjects:	Amphibia Animal biology Animals Biochemistry, Molecular Biology Biodiversity Cell Nucleus - genetics DNA, Mitochondrial - genetics Genome, Mitochondrial Genomics Hybridization, Genetic Introgression Life Sciences Mitochondria - genetics Phylogenetic network Phylogenomics Phylogeny Populations and Evolution RNAseq Salamandridae Transcriptome - genetics Urodela - classification Urodela - genetics Vertebrate Zoology
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Summary:	[Display omitted] •We present the first family-wide phylogenomic dataset for the Salamandridae.•Transcriptomic and mitochondrial analyses recover a new position for Salamandrina.•Transcriptomic data confirm mito-nuclear discordances in several groups of newts.•Ancient introgressive hybridization likely generated these discordances. 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 Ichthyos
ISSN:	1055-7903 1095-9513