Rooting the tree of life: the phylogenetic jury is still out
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This article aims to shed light on difficulties in rooting the tree of life (ToL) and to explore the (sociological) reasons underlying the limited interest in accurately addressing this fundamental issue. First, we briefly review the difficulties plaguing phylogenetic inference and the ways to improve the modelling of the substitution process, which is highly heterogeneous, both across sites and over time. We further observe that enriched taxon samplings, better gene samplings and clever data removal strategies have led to numerous revisions of the ToL, and that these improved shallow phylogenies nearly always relocate simple organisms higher in the ToL provided that long-branch attraction artefacts are kept at bay. Then, we note that, despite the flood of genomic data available since 2000, there has been a surprisingly low interest in inferring the root of the ToL. Furthermore, the rare studies dealing with this question were almost always based on methods dating from the 1990s that have been shown to be inaccurate for much more shallow issues! This leads us to argue that the current consensus about a bacterial root for the ToL can be traced back to the prejudice of Aristotle's Great Chain of Beings, in which simple organisms are ancestors of more complex life forms. Finally, we demonstrate that even the best models cannot yet handle the complexity of the evolutionary process encountered both at shallow depth, when the outgroup is too distant, and at the level of the inter-domain relationships. Altogether, we conclude that the commonly accepted bacterial root is still unproven and that the root of the ToL should be revisited using phylogenomic supermatrices to ensure that new evidence for eukaryogenesis, such as the recently described Lokiarcheota, is interpreted in a sound phylogenetic framework.
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The site-heterogeneous CAT model, despite outcompeting any site-homogeneous model, is not immune to reconstruction artifacts.
“Nonetheless, our observations with different sub-samplings of the sponge classes indicate that the site-heterogeneous CAT model, despite outcompeting any site-homogeneous model, is unsurprisingly not immune to reconstruction artifacts [23, 32].”
From A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals (2017) · cites this paper as [23]
Section 7 reports that CAT-based site-heterogeneous models performed slightly better than the site-homogeneous models tested, but all became sensitive to long-branch attraction as outgroup distance increased. Section 3 also says the CAT model can be inconsistent under heteropecilly. These passages support its vulnerability to reconstruction artifacts, but not the claim that it outcompetes *any* site-homogeneous model. (LLM, conf=0.85)
Experimental — accuracy not yet measuredCommonly applied phylogenetic models do not account for a wide array of factors that are known to cause positively misleading phylogenetic estimates when overlooked.
“While phylogenomics has revolutionized our understanding of the tree of life, commonly applied phylogenetic models do not account for a wide array of factors that are known to cause positively misleading phylogenetic estimates when overlooked18,19.”
From Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding (2021) · cites this paper as [18]
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Javaux, E. J., & Lepot, K. (2018) · Earth-Science Reviews · doi:10.1016/j.earscirev.2017.10.001 · Cited by 158 · see citing works
Redmond, A. K., & McLysaght, A. (2021) · Nature Communications · doi:10.1038/s41467-021-22074-7 · Cited by 139 · see citing works
Sporulation, bacterial cell envelopes and the origin of life
Tocheva, E. I., Ortega, D. R., & Jensen, G. J. (2016) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2016.85 · Cited by 121 · see citing works
An estimate of the deepest branches of the tree of life from ancient vertically evolving genes
Moody, E. R., Mahendrarajah, T. A., Dombrowski, N., Clark, J. W., Petitjean, C., Offre, P., Szöllősi, G. J., Spang, A., & Williams, T. A. (2022) · eLife · doi:10.7554/elife.66695 · Cited by 95 · see citing works
Phylogenetic Signal, Congruence, and Uncertainty across Bacteria and Archaea
Martinez-Gutierrez, C. A., & Aylward, F. O. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab254 · Cited by 95 · see citing works
ATP synthase evolution on a cross-braced dated tree of life
Mahendrarajah, T. A., Moody, E. R. R., Schrempf, D., Szánthó, L. L., Dombrowski, N., Davín, A. A., Pisani, D., Donoghue, P. C. J., Szöllősi, G. J., Williams, T. A., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42924-w · Cited by 86 · see citing works
“The presence of all four subunits in Bacteria is consistent with ideasfor a root of the universaltree within Bacteria 68 – 70 .”
BackgroundNew substitution models for rooting phylogenetic trees
Williams, T. A., Heaps, S. E., Cherlin, S., Nye, T. M. W., Boys, R. J., & Embley, T. M. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0336 · Cited by 61 · see citing works
Relative Time Constraints Improve Molecular Dating
Szöllõsi, G. J., Höhna, S., Williams, T. A., Schrempf, D., Daubin, V., & Boussau, B. (2022) · Systematic Biology · doi:10.1093/sysbio/syab084 · Cited by 23 · see citing works
- Authors
- Gouy, R., Baurain, D., & Philippe, H.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- University of Liège (BE)
- Corresponding author
- Philippe, Hervé
- Venue
- Philosophical Transactions of the Royal Society B: Biological Sciences
- Publisher
- The Royal Society
- Published
- 2015-09-26
- Volume
- 370
- Issue
- 1678
- Pages
- 20140329
- ISSN
- 0962-8436 (ISSN-L)
- 1471-2970
- PMC
- PMC4571568
- OpenAlex
- W2140742875
- Cited by
- 96
- References
- 94
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 4 · 2023: 11 · 2022: 12 · 2021: 12 · 2020: 9 · 2019: 6 · 2018: 13 · 2017: 10 · 2016: 5 · 2015: 4
- FWCI
- 1.03
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Philosophical Transactions of the Royal Society B Biological Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- ORBi (University of Liège) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protist diversity and phylogeny
- Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
- Keywords
- phylogenetic inference, long-branch attraction, substitution models, taxon sampling, Great Chain of Being, eukaryotic origin, supermatrices, phylogenomics, archaea, prokaryotes
- MeSH terms
- Animals, Eukaryotic Cells, Models, Genetic, Phylogeny, Prokaryotic Cells
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