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Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life

Abstract

Much progress has been achieved in disentangling evolutionary relationships among species in the tree of life, but some taxonomic groups remain difficult to resolve despite increasing availability of genome-scale data sets. Here we present a practical approach to studying ancient divergences in the face of high levels of conflict, based on explicit gene genealogy interrogation (GGI). We show its efficacy in resolving the controversial relationships within the largest freshwater fish radiation (Otophysi) based on newly generated DNA sequences for 1,051 loci from 225 species. Initial results using a suite of standard methodologies revealed conflicting phylogenetic signal, which supports ten alternative evolutionary histories among early otophysan lineages. By contrast, GGI revealed that the vast majority of gene genealogies supports a single tree topology grounded on morphology that was not obtained by previous molecular studies. We also reanalysed published data sets for exemplary groups with recalcitrant resolution to assess the power of this approach. GGI supports the notion that ctenophores are the earliest-branching animal lineage, and adds insight into relationships within clades of yeasts, birds and mammals. GGI opens up a promising avenue to account for incompatible signals in large data sets and to discern between estimation error and actual biological conflict explaining gene tree discordance.

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Figure 1: Null morphological hypothesis (H0) and all 14 possible alternative trees for the five major lineages in Otophysi.
Figure 2: Gene genealogy interrogation (GGI) applied to phylogenomic data sets to test alternative hypotheses.
Figure 3: Otophysan phylogeny based on the concatenation analysis of 231 protein genes with minimal missing information.

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Acknowledgements

We dedicate this contribution in honour and memory of our friend and valued colleague Richard Vari whose untimely death has left a huge lacuna in the world of otophysan systematics. We thank D. Maddison, for helping with the MDS analyses in Mesquite, and R. Rivero, for helping with illustrations. We also thank S. Edwards and T. Warnow for providing extensive comments on earlier versions of the paper. J. P. Sullivan kindly provided a photograph for Citharinoidei. This work was supported by National Science Foundation (NSF) grants (DEB-147184, DEB-1541491) to R.B.R., (DEB-1457426 and DEB-1541554) to G.O., (DEB-0315963 and DEB-1023403) to J.W.A., and (DEB-1350474) to L.J.R. This project was also funded by the Opportunity Research Program between George Washington University and the Natural History Museum (Smithsonian) to G.O. and R.V and the Smithsonian Peter Buck fellowship to R.B.R.

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D.A., R.B.R., R.V. and G.O. planned the project; R.B.R., K.K and G.O. conducted the pilot experiment; D.A. and R.B.R. carried out the experiments and collected the data; D.A., R.B.R., L.J.R., and G.O. conceived the GGI method; D.A. and R.B.R. analysed data; J.W.A., J.L., M.L.J.S., and M.H.S. collected, identified and curated the fish specimens examined; R.B.R., D.A. and G.O. wrote the paper and all other authors contributed to the writing.

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Correspondence to Ricardo Betancur-R..

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Supplementary Methods, Supplementary Notes, Supplementary Figures 1–7 and Supplementary Tables 1–8. (PDF 1912 kb)

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Arcila, D., Ortí, G., Vari, R. et al. Genome-wide interrogation advances resolution of recalcitrant groups in the tree of life. Nat Ecol Evol 1, 0020 (2017). https://doi.org/10.1038/s41559-016-0020

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