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Incongruence in the phylogenomics era

Nature Reviews Genetics volume 24, pages 834–850 (2023)Cite this article

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Abstract

Genome-scale data and the development of novel statistical phylogenetic approaches have greatly aided the reconstruction of a broad sketch of the tree of life and resolved many of its branches. However, incongruence — the inference of conflicting evolutionary histories — remains pervasive in phylogenomic data, hampering our ability to reconstruct and interpret the tree of life. Biological factors, such as incomplete lineage sorting, horizontal gene transfer, hybridization, introgression, recombination and convergent molecular evolution, can lead to gene phylogenies that differ from the species tree. In addition, analytical factors, including stochastic, systematic and treatment errors, can drive incongruence. Here, we review these factors, discuss methodological advances to identify and handle incongruence, and highlight avenues for future research.

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Fig. 1: Incongruence at different levels of genomic organization.
Fig. 2: Major biological factors that contribute to incongruence.
Fig. 3: Analytical factors can contribute to incongruence at every step in a phylogenomic workflow.

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Acknowledgements

J.L.S. and A.R. were funded by the Howard Hughes Medical Institute through the James H. Gilliam Fellowships for Advanced Study Program. Research in A.R.’s lab is supported by grants from the National Science Foundation (DEB-2110404), the National Institutes of Health/National Institute of Allergy and Infectious Diseases (R01 AI153356), and the Burroughs Wellcome Fund. A.R. acknowledges support from a Klaus Tschira Guest Professorship from the Heidelberg Institute for Theoretical Studies and from a Visiting Research Fellowship from Merton College of the University of Oxford. X.X.S. was supported by the National Key R&D Program of China (2022YFD1401600). Y.L. was supported by Shandong University Outstanding Youth Fund (62420082260514). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Howards Hughes Medical Institute and the Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA, USA

    Jacob L. Steenwyk

  2. Department of Biological Sciences, Vanderbilt University, Nashville, TN, USA

    Jacob L. Steenwyk & Antonis Rokas

  3. Vanderbilt Evolutionary Studies Initiative, Vanderbilt University, Nashville, TN, USA

    Jacob L. Steenwyk & Antonis Rokas

  4. Institute of Marine Science and Technology, Shandong University, Qingdao, China

    Yuanning Li

  5. Guangdong Laboratory for Lingnan Modern Agriculture, Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, China

    Xiaofan Zhou

  6. Key Laboratory of Biology of Crop Pathogens and Insects of Zhejiang Province, Institute of Insect Sciences, Zhejiang University, Hangzhou, China

    Xing-Xing Shen

  7. Heidelberg Institute for Theoretical Studies, Heidelberg, Germany

    Antonis Rokas

Authors
  1. Jacob L. Steenwyk
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  2. Yuanning Li
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  3. Xiaofan Zhou
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  4. Xing-Xing Shen
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  5. Antonis Rokas
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Contributions

All authors researched the literature, contributed substantially to discussions of the content, and reviewed and/or edited the manuscript before submission. J.L.S. and A.R. wrote the article.

Corresponding author

Correspondence to Antonis Rokas.

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Competing interests

J.L.S. is a scientific adviser for WittGen Biotechnologies and an adviser for ForensisGroup. A.R. is a scientific consultant for LifeMine Therapeutics. The other authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Genetics thanks Thijs J.G. Ettema, who co-reviewed with Daniel Tamarit, and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Glossary

Convergent molecular evolution

Independent evolution of similar or identical molecular changes (for example, gene deletions, nucleotide substitutions, gene order rearrangements) in organisms from different lineages that exhibit similar adaptations.

Evolutionary radiation

The occurrence of an elevated rate of speciation events in a narrow window of evolutionary time.

Heterotachy

The phenomenon of changes in the evolutionary rate of a nucleotide or amino acid sequence through time.

Hidden orthology

Undetected orthologous relationships of genes.

Hidden paralogy

Orthologous groups of genes that contain orthologues and paralogues (inparalogues and outparalogues) stemming from asymmetric patterns of duplication and loss.

Horizontal gene transfer

Also known as lateral gene transfer. The transfer of genetic material between organisms of the same or different species through non-reproductive means.

Hybridization

The interbreeding of two distinct species or lineages.

Inparalogues

Lineage-specific or species-specific paralogues wherein the duplication event occurred after divergence from a reference common ancestor.

Introgression

The interbreeding of two distinct species or lineages, followed by backcrossing with one of the parental species.

Long-branch attraction

The inaccurate inference of taxa with high evolutionary rates (giving rise to long branches in their phylogenetic trees) as closely related.

Model of sequence evolution

Also known as the substitution model. Markov models that describe rates of nucleotide or amino acid substitutions in a locus during evolution.

Partial or incomplete taxon coverage

The lack of sequences (either because they are genuinely absent or because they were not collected) from particular taxa in a group of orthologous genes.

Phylogenetic irreproducibility

Lack of reproducibility of a tree topology between two replicate tree inferences using the same software parameters (for example, same model of sequence evolution or starting seed).

Phylogenetic networks

Graphs of evolutionary relationships that, in addition to depicting the splitting of lineages, also depict the merging of lineages (due to events such as hybridization and convergent molecular evolution or due to different gene tree topologies).

Taxon sampling

Which and how many taxa are selected for a phylogenetic analysis.

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Steenwyk, J.L., Li, Y., Zhou, X. et al. Incongruence in the phylogenomics era. Nat Rev Genet 24, 834–850 (2023). https://doi.org/10.1038/s41576-023-00620-x

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