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Contentious relationships in phylogenomic studies can be driven by a handful of genes

Nature Ecology & Evolution volume 1, Article number: 0126 (2017) Cite this article

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Abstract

Phylogenomic studies have resolved countless branches of the tree of life, but remain strongly contradictory on certain, contentious relationships. Here, we use a maximum likelihood framework to quantify the distribution of phylogenetic signal among genes and sites for 17 contentious branches and 6 well-established control branches in plant, animal and fungal phylogenomic data matrices. We find that resolution in some of these 17 branches rests on a single gene or a few sites, and that removal of a single gene in concatenation analyses or a single site from every gene in coalescence-based analyses diminishes support and can alter the inferred topology. These results suggest that tiny subsets of very large data matrices drive the resolution of specific internodes, providing a dissection of the distribution of support and observed incongruence in phylogenomic analyses. We submit that quantifying the distribution of phylogenetic signal in phylogenomic data is essential for evaluating whether branches, especially contentious ones, are truly resolved. Finally, we offer one detailed example of such an evaluation for the controversy regarding the earliest-branching metazoan phylum, for which examination of the distributions of gene-wise and site-wise phylogenetic signal across eight data matrices consistently supports ctenophores as the sister group to all other metazoans.

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Figure 1: A schematic representation of our approach for quantifying and visualizing phylogenetic signal in a phylogenomic data matrix.
Figure 2: Distributions of phylogenetic signal for 17 contentious branches in plant, animal and fungal phylogenomic data matrices.
Figure 3: Quantification of the effect of the removal of tiny amounts of data on the branch’s topology for 17 contentious branches in plant, animal and fungal phylogenomic data matrices.
Figure 4: Tiny amounts of data exert decisive influence in the resolution of certain contentious branches in phylogenomic studies.
Figure 5: The distribution of phylogenetic signal for three alternative topological hypotheses on the earliest-branching metazoan lineage.

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Acknowledgements

We thank members of the Rokas laboratory, and in particular X. Zhou, for discussions and comments. We also thank M. Chen for providing the animal phylogenomic data matrix and J. Leebens-Mack for providing further information about the plant data matrix. This work was conducted in part using the resources of the Advanced Computing Center for Research and Education (ACCRE) at Vanderbilt University, of the UW-Madison Center for High Throughput Computing, and of the CIPRES Science Gateway. This work was supported by the National Science Foundation (DEB-1442113 to A.R.; DEB-1442148 to C.T.H.), in part by the DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02- 07ER64494), the USDA National Institute of Food and Agriculture (Hatch project 1003258 to C.T.H.), and the National Institutes of Health (NIAID AI105619 to AR). C.T.H. is a Pew Scholar in the Biomedical Sciences, supported by the Pew Charitable Trusts.

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Authors and Affiliations

  1. Department of Biological Sciences, Vanderbilt University, Nashville, 37235, Tennessee, USA.

    Xing-Xing Shen & Antonis Rokas

  2. Laboratory of Genetics, Genome Center of Wisconsin, DOE Great Lakes Bioenergy Research Center, Wisconsin Energy Institute, J. F. Crow Institute for the Study of Evolution, University of Wisconsin-Madison, Madison, 53706, Wisconsin , USA.

    Chris Todd Hittinger

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Contributions

X.X.S. and A.R. conceived and designed the study. X.X.S., C.T.H. and A.R. were responsible for acquisition of data, and analysis and interpretation of data. The manuscript was drafted by X.X.S. and A.R., with critical revision by X.X.S., C.T.H. and A.R.

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Correspondence to Antonis Rokas.

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Shen, XX., Hittinger, C. & Rokas, A. Contentious relationships in phylogenomic studies can be driven by a handful of genes. Nat Ecol Evol 1, 0126 (2017). https://doi.org/10.1038/s41559-017-0126

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